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HPV Vaccine Acceptability by Latino Parents: A Comparison of U.S. and Salvadoran Populations
J Pediatr Adolesc Gynecol (2009) 22:205e215
Original Study HPV Vaccine Acceptability by Latino Parents: A Comparison of U.S. and Salvadoran Populations Rebecca Podolsky, BA, Miriam Cremer, MD, MPH, Jessica Atrio, MD, Tsivia Hochman, MS, and Alan A. Arslan, MD New York University School of Medicine, Department of Obstetrics & Gynecology and Department of Biostatistics, New York, NY, USA; Basic Health El Salvador, San Salvador, El Salvador
Abstract. Study Objective: To characterize and compare acceptability of human papillomavirus (HPV) vaccination by Latino parents at an urban medical center in the United States and a community hospital in El Salvador. Design: After reading an information sheet on HPV, 148 subjects at Bellevue Hospital in New York City and 160 subjects at Hospital Nacional de Santa Gertrudis in San Vicente, El Salvador, completed a survey. Results were analyzed using chi-square, Fisher’s exact test, and Student’s t-tests. Results and Conclusions: Parental acceptance of HPV vaccination was higher in a sample of Salvadoran subjects than in a sample of U.S. Latinas (P ! 0.001 for daughters and sons). Reasons for objecting to HPV vaccination differ in the two locations. There are important differences between Salvadoran and U.S. subjects. Salvadorans are more accepting of HPV vaccination, and parental acceptance is unlikely to be a barrier to widespread vaccination in El Salvador. Targeted educational materials are needed in both locations.
Adddress correspondence to: Miriam Cremer, MD, NYU School of Medicine Department of Obstetrics and Gynecology, 550 First Avenue, New York, NY 10016.; E-mail: [email protected]
sexually active adults will be infected with HPV during their lifetimes.2,3 The Food and Drug Administration approved the first multivalent HPV vaccine in 2006. This vaccine prevents acquisition of subtypes 6, 11, 16, and 18, which together cause approximately 90% of genital warts and 70% of cervical cancers.3 In order for this vaccine to be maximally effective clinically, widespread vaccination of HPV-naı¨ve individuals is required. Practically, this means vaccinating children before the onset of sexual activity. According to the 2005 Youth Risk Behavior Survey, 29.3% of females and 39.3% of males in the United States have had sexual intercourse by the time they are in ninth grade.4 Thus, assessing the attitudes of parents about the HPV vaccine is critical because they could constitute a major barrier to successful implementation of widespread HPV vaccination. Several previous studies have looked at the question of acceptability of the HPV vaccine among parents in various populations.5,6,7 In the United States, Latina women are among the least likely to receive regular Papanicolaou (Pap) screenings8 and are among the most likely to be diagnosed with and die of cervical cancer.9 However, there is a dearth of information about acceptability in low-income Latino populations in the United States, even as this is a population that stands to benefit greatly from HPV vaccination.10 There is even less research into how the vaccine will be received in developing countries, where 83% of cervical cancer cases occur.11 In El Salvador, where this survey was administered, in the year 2000 there were 40.6 cases diagnosed per 100,000 women, compared to 8.7 per 100,000 in the United States.12 As in the United States, El Salvador has a high rate of adolescent sexual activity, with 88% of females reporting their first coitus before age 1913 and 100 births per 1000 women aged 15 to 19.14 Thus, widespread vaccination of children will
Ó 2009 North American Society for Pediatric and Adolescent Gynecology Published by Elsevier Inc.
1083-3188/09/$36.00 doi:10.1016/j.jpag.2008.05.010
Key Words. Human papillomavirus (HPV) vaccine— Acceptability—Latino
Introduction Human papillomavirus (HPV), the causative agent in genital warts and cervical carcinoma, is one of the most common sexually transmitted infections in the United States1 and worldwide.2 At least 20 million Americans are currently infected with HPV and nearly half of Sources of Support: Funding came from the NYU School of Medicine’s Department of Obstetrics and Gynecology and from Basic Health El Salvador, a nongovernmental organization dedicated to improving cervical cancer screening and prevention in El Salvador.
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be necessary to ensure maximal effectiveness of the vaccine in El Salvador. Rates of cervical cancer have decreased in the developed world since the successful implementation of widespread Pap screening. In the developing world, such screening is less feasible because of cost and health care infrastructure requirements, so the rates of cervical cancer remain high. The public health system in El Salvador makes Pap tests available, but one study found that insufficient supplies, loss of samples, slow turnaround time, a reading backlog, and poor quality control greatly decreased the efficacy of screening efforts.15 Indeed, the rates of abnormal Pap test results in the United States and El Salvador are nearly equal, but Salvadoran women have a much higher incidence of and mortality rate from cervical cancer.16,17 This fact highlights the apparent failure of current screening methods in that country, including Pap tests. Thus the HPV vaccine has great potential to decrease the incidence of cervical cancer in countries like El Salvador. An improved understanding of how the Salvadoran population will receive this vaccine is critical to ensuring that when the vaccine becomes available in that country, it can be maximally effective. This study offers a comparison between two economically disadvantaged Latino populations, one of which has access to the HPV vaccine and one of which does not. Subjects at both sites can safely be described as economically disadvantaged by virtue of their having sought care at our two recruitment sites. Bellevue is a municipal hospital whose patients are either uninsured or insured by state or federal insurance programs designed to cover low-income families. Subjects recruited at the Hospital Nacional de Santa Gertrudis in El Salvador came from the surrounding semirural and rural areas where an estimated 50% of Salvadorans live in poverty and close to 25% live in extreme poverty. Of the country’s approximately 6,000,000 inhabitants, as of 2002, 80%were covered by the public health system.18 The goals of this study were to characterize levels of parental acceptance of HPV vaccination for children aged 8 to 18 in these two populations and to assess parents’ reasons for refusing HPV vaccination for their children. The two study populations share a common language and religious background and, to some degree, a cultural background.* The purpose of comparing these two populations is to provide insight into the potential impact of differences such as vaccine availability, media attention, attitudes about vaccines in general, and knowledge about HPV and vaccine acceptability. Materials and Methods Mothers of children between the ages of 8 and 18 were approached in the waiting rooms of the Bellevue
Hospital pediatric clinic in New York City and the Hospital Nacional de Santa Gertrudis (HNSG) in San Vicente, El Salvador. Potential subjects were asked the ages of their children and whether they would be willing to complete a survey about the HPV vaccine. Eligibility criteria were slightly different at the two sites because of the low level of literacy in the Salvadoran community. At both sites, subjects had to be at least 18 years old and the parent or guardian of a child between the ages of 8 and 18. At Bellevue, subjects had to be able to read and write either English or Spanish because the survey was self-administered there, whereas at HNSG, literacy was not a requirement; a researcher administered the survey. No compensation was provided for participation in the survey at either site. It is certainly possible that there were potential subjects in the Bellevue population who could not read and write. The ability to read and write was an inclusion criterion at this site, so these people may have been among the small number of refusals. Researchers did not press those who declined to participate about their reasons for refusing. The research instrument consisted of a 10-item fact sheet about HPV (Fig. 1) that was developed by the research team and an anonymous, 28-item survey (Fig. 2). Many of the questions in the survey (10 and 20 through 28) were taken or adapted from a questionnaire developed at the University of Texas.19 The survey was translated into Spanish by fluent speakers of the language with the help of a Salvadoran physician involved in the study. Question 15, which asks about taking the advice of the doctor about vaccines, and question16, which asks about vaccination requirements, were omitted by researchers when administering the survey in El Salvador. Nationwide vaccination campaigns are carried out several times each year there, but the vaccines are not usually administered by doctors, and requirements do not exist as they do in the United Stares. It was believed that Salvadoran subjects would not be able to answer these questions appropriately. This study was approved by the Institutional Review Board at the New York University School of Medicine and by the Ministry of Health in El Salvador. We hypothesized that acceptance would differ in the two study populations. Based on the literature, we estimated a 70% parental acceptance rate of HPV vaccination for daughters in the Bellevue group and an 85% acceptance rate in the HNSG group. We based our hypothesis on the results of two studies: one by Davis and colleagues20 that looked at parental acceptance in a U.S. population before and after an intervention that consisted of a fact sheet about HPV; and the other by Lazcano-Ponce and colleagues that looked at acceptance among mothers in Cuernavaca, Mexico.21 We estimated a sample size of 134 per group to detect a difference of 15% between the two groups based on
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Facts about Human Papillomavirus (HPV) 1. HPV is spread by sexual activity. 2. HPV is very common (at least 50 in their lives).
of people who have sex will have HPV at some point
3. Most people who have HPV don’t know they have it. 4. There are many kinds of HPV and not all of them cause health problems. 5. Only some kinds of HPV cause health problems like genital warts or cervical cancer. 6. Most women who have HPV will NOT develop cervical cancer, and will likely get rid of the virus on their own without medical treatment. 7. Condoms do not always protect against the spread of HPV. 8. You can get HPV without having sexual intercourse (penetration sex); it is transmitted by genital -to-genital co ntact, not by the exchange of bodily fluids. 9. There is no cure for HPV, but there are treatments for problems such as genital warts and cervical cancer that are caused by HPV. There is a new vaccine against the kinds of HPV that most often cause cervical cancer and genital warts. This vaccine is most effective if given before a person becomes sexually active. The HPV vaccine is now available for girls age nine and older.
Figure 1. Fact Sheet Read by Subjects Prior to Completing Questionnaire
80% power and an alpha level of 0.05. Descriptive statistics were calculated on all survey items. Subgroups within the study population were compared using chi-square, Fisher’s exact test, and Student’s t-tests. Results Of the Salvadoran women at Hospital Nacional de Santa Gertrudis, 188 were asked to participate in the study. Of these, 9 (4.7%) refused, and 19 (10.1%) were ineligible. The number of women who completed the survey was 160. At Bellevue, a total of 229 people were approached as potential participants. Of these, 17 (7.4%) refused, and 12 (5.2%) were ineligible. Ultimately, 200 people completed the survey, 153 of whom (76.5%) were Latino. For the purposes of this study, we chose to include only Latino subjects. Additionally, 5 of the 153 Latino Bellevue subjects were male. We chose to exclude them from the analysis. Therefore, the Bellevue group contained 148 subjects. Demographic data for both groups are listed and compared in Table 1. In summary, Salvadorans were much less familiar with HPV and the HPV vaccine than were Bellevue subjects. Of the Salvadoran subjects, 70% indicated that they had never heard of HPV or the vaccine before reviewing the fact sheet accompanying this survey, compared to 12.2% of Bellevue subjects (P ! 0.0001). The Salvadoran study population had lower levels of education than did the Bellevue group. Most notably, 18.8% of
Salvadoran study subjects had never been to school; none of the Bellevue subjects fell into this category. Of the Bellevue subjects, 46.6% were graduates of high school or higher education; 11.9% of Salvadoran subjects were in that category (chi-square 45.48, P ! 0.001). Salvadoran subjects had a higher mean number of children than did Bellevue subjects (4.0 vs. 2.4, t 5 9.65, P ! 0.001), and their children were older than the children of Bellevue subjects (14.2 years vs. 12.7 years, P ! 0.02). Bellevue subjects were more likely to report having had a gynecologic exam within the past 1 to 2 years than were Salvadoran subjects (92.6% vs. 62.5%, P ! 0.0001). Despite this discrepancy, Salvadoran subjects were approximately twice as likely as Bellevue subjects to report a history of abnormal cytology (33.8% vs. 16.3%, chi-square 5 12.35, P 5 0.002), although some of the abnormal test results reported by subjects in both groups may have been due to inflammation or infection. Data from both El Salvador and the United States that measured rates of abnormal Pap tests on the basis of cytologic diagnosis yielded much lower incidences than did data based on patient self-report. Data from the Salvadoran Ministry of Health indicate that in 2005, 3.5% of Pap tests done in that country were read as abnormal. Studies based on pathology results done in the United States cite rates of abnormal cervical cytology between 3% and 10%, depending on the study population.22 Despite this, one nationwide study done in the United States in 2004 found that 20% of women surveyed reported at least
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HPV Vaccine Survey 1. Please mark one answer: __I understood everything I just read about HPV and the HPV vaccine…………..1 __I understood some of what I just read about HPV and the HPV vaccine………..2 __I understood very little of what I just read about HPV and the HPV vaccine…..3 __I did not understand what I just read about HPV and the HPV vaccine……….4 2. Please mark one answer: __I already knew all of what I just read about HPV and the HPV vaccine………..1 __I already knew some of what I just read about HPV and the HPV vaccine…….2 __I have heard of HPV but didn’t know very much of what I just read…………3 __I have never heard of HPV before reading the information sheet……………..4 Demographic Information: 3. Are you:
__Female…………………………………………………………..1 __Male…………………………………………………………….2
4. How old are you?
________
5. Race (mark one answer): __Hispanic…………………………………………………………………1 __White/Caucasian………………………………………………………..2 __Black/African American………………………………………………..3 __Asian/Pacific Islander…………………………………………………..4 __Native American/Aleutian Eskimo……………………………………..5 __Other (_________________________)………………………………..6 6. What language do you usually speak at home? __English………………………………………………………………….1 __Spanish………………………………………………………………….2 __Chinese………………………………………………………………….3 __Korean…………………………………………………………………..4 __Russian……………………………………………………………….…5 __French…………………………………………………………………..6 __Bengali………………………………………………………………….7 __Tagalog…………………………………………………………………8 __Polish…………………………………………………………………...9 __Hindi……………………………………………………………………10 __Urdu…………………………………………………………………….11 __Other language (______________________________________)…….12 7. Religion (mark one answer): __Catholic…………………………………………………………………1 __Protestant……………………………………………………………….2 __Jewish………………………………………………………………….. 3 __Muslim………………………………………………………………….4 __Hindu…………………………………………………………………...5 __Jehovah’s Witness……………………………………………………...6 __No religion……………………………………………………………...7 __Other (___________________________)……………………………..8
Figure 2. H2PV Vaccine Survey
one abnormal Pap test result.23,24 The discrepancy between subject self-report and data based on cytology may be a result of the lack of understanding among women of the purpose of Pap screening and of the various components of a gynecological exam.25
Acceptance of HPV vaccination for sons, daughters, and oneself differs in the two study populations (Table 2). It is notable that in both groups, but more strikingly in the Bellevue population, more subjects would accept vaccination for themselves than for either their sons or
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8. What is your highest level of education? __Elementary School………………………………………………1 __Some high school………………………………………………..2 __High school graduate/GED……………………………………...3 __Associate’s Degree………………………………………………4 __Some college…………………………………………………….5 __College Graduate……………………………………………….. 6 __Graduate School…………………………………………………7 9. How many children do you have? Age/sex of children (Fill in age and circle sex) _____
male…1
female…2
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male…1
female…2
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male…1
female…2
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male…1
female…2
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male…1
female…2
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male…1
female…2
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male…1
female…2
10. Did your children receive all vaccinations that were offered by their doctor/nurse? (mark one answer) __Yes…1_ _No…2 __I don’t know…3
11. If your child has not received all of his/her vaccines, why not? (choose one) __We were living in another country……………………1 __We couldn’t come to doctor/didn’t have a doctor…….2 __I was concerned about side effects……………………3 __I didn’t think my child would get the disease…………4 __I believed the disease was not serious…………………5 __I was concerned about the cost of the shot…………….6 __Other reason (Specify_______________________)…..7 12. Did your children experience any side effects or problems with any vaccinations? (mark one answer) __Yes…1 __No…2 __I don’t know…3 If yes, please describe:____________________________________________________ _ Please circle the answer choice that best describes your feelings about the question. 13. I believe vaccines are important to the health of my child. Strongly Agree…1 Agree…2 Neutral…3 Disagree…4
Strongly Disagree…5
Figure 2. (Continued)
their daughters. At Bellevue, 78.4% of subjects would accept the HPV vaccine for themselves, whereas 68.2% and 58.7% would consent to HPV vaccination for their daughters and sons, respectively. Of the Bellevue subjects, 16.2% said they would accept the vaccine for themselves but were unsure about or would refuse vaccination for their daughters. Only 3.75% of Salvadoran subjects responded this way. The average age
among the subgroup at Bellevue was 37.12 years, and in El Salvador 38.5 years, compared to 37.5 years and 39.2 years in the Bellevue and Salvadoran populations, respectively. The reasons given for being unsure about or refusing HPV vaccination for one’s daughters also reflected the reasons most commonly given by the study population as a whole. These reasons are discussed later.
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Podolsky et al: HPV Vaccine Acceptability by Latino Parents 14. I am concerned that some vaccines are not safe/not good for my child. Strongly Agree…1 Agree…2 Neutral…3 Disagree…4 Strongly Disagree…5 15. I always take the advice of my child’s doctor about vaccines. Strongly Agree…1 Agree…2 Neutral…3 Disagree…4 Strongly Disagree…5 16. I don’t like immunization requirements because parents know what is best for their child. Strongly Agree…1 Agree…2 Neutral…3 Disagree…4 Strongly Disagree…5 17. I trust older vaccines more than I trust new vaccines . Strongly Agree…1 Agree…2 Neutral…3 Disagree…4
Strongly Disagree…5
18. For women only: Do you have a gynecologic exam performed every 1-2 years? (mark one answer) __Yes…1 __No…2_ _I don’t know…3
19. If no, why not? (Choose one) __Don’t think I need them every year………………………………….1 __Don’t have health insurance…………………………………………2 __Don’t want to go to the doctor that often……………………………3 __Other (please describe________________________________)……4 20. Have you ever had an abnormal PAP (Papanicolaou) test/smear? (mark one answer) _Yes…1 __No…2 __I don’t know…3 21. Have you ever had colposcopy? (a procedure that your doctor uses to find the cause of a Pap smear abnormality.) (mark one answer) _Yes…1 __No…2 __I don’t know…3 22. Have you ever had a hysterectomy (surgery to remove the uterus or “womb”? (mark one answer) _Yes…1 __No…2 __I don’t know…3 23. If the HPV vaccine were to work at any age, would you get the vaccine for yourself? (mark one answer) _Yes…1 __No…2 __I don’t know…3 24. If you marked “No,” why not? __Because it is a new vaccine………………………….………….…..……1 __Because I don’t think I am at risk for HPV………………………....…...2 __Because I don’t know enough about HPV/I want to talk about the vaccine with my doctor first………………….…….…..…..3 __Another reason..(Please state reason:_______________________)…......4 If you have a daughter between the ages of 8 and 18, please answer questions 25 and 26. If you do not have a daughter in this age group, please skip to question 27. 25. Would you give consent for your daughter to receive the HPV vaccine? (mark one answer) _Yes…1_ _No…2 __I don’t know…3
Figure 2. (Continued)
Subjects who responded that they were unsure or that they would refuse HPV vaccination for their child or children were asked about their reasons for doing so (Table 3). In both groups, the most commonly chosen reason from a list of possible choices was ‘‘Because I don’t know enough about HPV. I want to talk to my child’s doctor first’’ (42.5% at Bellevue; 40% in El Salvador). A smaller group in each location
expressed concern about the HPV vaccine’s being new (17% at Bellevue; 20% in El Salvador). Subjects at Bellevue were more likely than their Salvadoran counterparts to express the concern that consenting to HPV vaccination would be interpreted as tacit approval of early sexual activity (14.9% vs. 0%). Bellevue subjects were also more likely to feel that their children were not at risk for HPV (12.7% vs. 5%).
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26. If you marked“No,” or“I don’t know,” why not? __Because it is a new vaccine ………………………… .………….…..……1 __Because I don’t think my daughter is at risk for HPV……………....2 __Because I don’t want the doctor talking to my daughter about sex/sexually transmitted infections……….……………………...……3 __Because if my daughter gets vaccinated against HPV, she might not use condoms when she has sex……………………… 4 __Because I don’t want my daughter to think it’s ok to start having sex if she gets this vaccine ………………………………………….…5 __Because I don’t know enough about HPV, I want to talk about the vaccine with my child’s doctor first………….…….…..…..6 __Another reason..(Please state reason:_______________________)…......7
If you have a son between the ages of 8 and 18, please answer questions 27 and 28. 27. Would you give consent for your son to receive the HPV vaccine? (mark one answer) __Yes…1 __No…2 __I don’t know…3 28. If you marked “No,” or “I don’t know,” why not? __Because it is a new vaccine ………………………….………….…..……1 __Because I don’t think my son is at risk for HPV………………….....2 __Because I don’t want the doctor talking to my son about sex/sexually transmitted infections ……….……………………...……3 __Because if my son gets vaccinated against HPV, he might not use condoms when he has sex……………..…………4 __Because I don’t want my son to think it’s ok to start having sex if he gets this vaccine………………….……………………….5 __Because I don’t know enough about HPV, I want to talk about the vaccine with my child’s doctor first………….………..….6 __Another reason..(Please state reason:_______________________)…....7 Thank you for your help!!
Figure 2. (Continued)
Attitudes about vaccines in general differ significantly in these two populations (Table 4). Of Salvadoran subjects, 72%, and of Bellevue subjects, only 31% disagreed with the statement ‘‘Some vaccines are not safe/not good for my child.’’ Subjects at Bellevue were more likely than were Salvadoran subjects to agree or feel neutral about the statement ‘‘I trust older vaccines more than new vaccines’’. At Bellevue, 24% of subjects agreed with the previous statement, 50% felt neutral, and 26% disagreed. In El Salvador, 13% agreed, 11% felt neutral, and 76% disagreed; most of those who disagreed indicated to the researchers that they trusted new vaccines more than older ones. Discussion Based on the results of this study, several conclusions can be drawn. First, parental acceptance of HPV vaccination is higher in El Salvador than in the United States. This finding supports both our initial hypothesis and the findings of similar studies looking at acceptance of HPV vaccination in the United States
and in developing countries. Second, there are some interesting differences in the reasons given for objecting to HPV vaccination for one’s children. Finally, attitudes about vaccines in general differ between the two study populations. There are many possible reasons for the different levels of acceptance of the HPV vaccine in the two populations: difference in the demographics of the two populations, a higher rate of abnormal cytology among Salvadoran women, the fact that the HPV vaccine is available to the Bellevue population and has not yet been approved in El Salvador, and a difference in the level of prior knowledge of HPV in the two populations. Salvadoran subjects tend to be less educated and less familiar with HPV than Bellevue subjects. As education campaigns about HPV and the HPV vaccine target the Salvadoran population, acceptance of the vaccine may change. Several studies have looked at the impact on acceptance of the HPV vaccine of providing information about HPV and the vaccine, and the results have been equivocal. One study, by
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Table 1. Demographic Characteristics of Participants on the Basis of Location of Survey Bellevue N 5 148
Characteristic
El Salvador N 5 160
Age (years), mean (SD) 37.5 (6.8) Familiarity with HPV and the HPV vaccine, n (%) Already knew everything on fact sheet 14 (9.5%) Already knew some of fact sheet 62 (41.9%) Had heard of HPV but did not know very much 54 (36.5%) Never heard of HPV before fact sheet 18 (12.2%) Highest level of education, n (%) No school 0 (0%) Elementary school 38 (25.7%) Some high school 41 (27.7%) High school/GED 42 (28.4%) Associate’s degree 7 (4.7%) Some college 11 (7.4%) College 8 (5.4%) Postgraduate 1 (0.7%) Proportion of high school graduates, n (%) Did not complete high school 79 (53.4%) Graduated from high school 69 (46.6%) Total number of children, mean (SD) 2.4 (1.1) Age of subjects’ children, mean (SD) 12.7 (5.5) Subject has had a gynecologic exam in the past 1-2 years Yes 137 (92.6%) No 9 (6.1%) Don’t know 2 (1.4%) Subject has history of abnormal PAP, n (%) Yes 24 (16.3%) No 116 (78.9%) Don’t know 7 (4.8%) Missing 1 (0.7%) Subject’s children have received all vaccines, n (%) Yes 144 (97.3%) No 3 (2.0%) Don’t know 1 (0.7%)
Dempsey and colleagues, found no significant increase in acceptance of HPV vaccination after the introduction of a fact sheet, despite the increased knowledge about HPV.26 However, another study, by Chan and colleagues, which also looked at parental acceptance of HPV vaccination before and after an information-based intervention, did find a statistically significant increase in acceptance of vaccination.27 Thus, from the literature it is difficult to predict what effect increasing knowledge will have on Salvadorans’ acceptance of HPV vaccination.
Statistical Test and Value
P Value
39.2 (7.4)
t value 5 2.06
0.040
4 (2.5%) 13 (8.1%) 31 (19.4%) 112 (70.0%)
N/A
! 0.0001
30 (18.8%) 95 (59.4%) 16 (10.6%) 6 (3.1%) 1 (0.6%) 1 (0.6%) 0 (0%)
N/A
! 0.0001
141 (88.1%) 19 (11.9%) 4.0 (1.9) 14.2 (5.4)
Chi-square 5 45.48
! 0.001
t value 5 9.65 N/A
! 0.0001 ! 0.02
100 (62.5%) 59 (36.9%) 1 (0.6%)
N/A
! 0.0001
54 (33.8%) 99 (61.9%) 7 (4.4%) 0 (0%)
Chi-square 5 12.35
0.002
149 (93.1%) 10 (6.3%) 1 (0.6%)
N/A
0.17
The HPV vaccine has not yet been approved in El Salvador, so it was not available when the subjects participated in this study. Bellevue Hospital had just obtained the vaccine when this study began enrollment, so it was available there. Salvadoran subjects were answering questions about a theoretical vaccine, so they may have been more focused on its benefits, whereas the Bellevue subjects were facing a more immediate and real decision. Because the vaccine is not yet available in El Salvador, no attention has been paid to the vaccine, positive or negative, that might
Table 2. Acceptance or Refusal of HPV Vaccination for Survey Participants and for Their Children by Location of Survey Bellevue (N 5 148) Yes
No
Self, n (%) 116 (78.4%) 13 (8.8%) Daughter 8-18 years old, n (%) 101 (68.2%) 14 (9.5%) Son 8-18 years old, n (%) * 27 (58.7%) 8 (17.4%)
I don’t know 19 (12.8%) 33 (22.3%) 11 (23.9%)
El Salvador (N 5 160) Yes
No
141 (88.1%) 5 (3.1%) 140 (87.5%) 7 (4.4%) 9 (87.6%) 3 (2.9%)
Chi-square P Value
I don’t know 14 (8.8%) 13 (8.1%) 10 (9.5%)
6.29 16.90 N/A
0.043 !0.001 !0.001
*Note: Having a son 8-18 was not an eligibility criterion, and only women with sons in this age group answered questions about HPV vaccination for boys. Thus, the number in this group is lower than the number in the total study group.
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Table 3. Reasons for Refusing or Being Unsure About Consenting to HPV Vaccination for Daughter by Location of Survey Bellevue N 5 47
Reason Because it is a new vaccine, n (%) Because I don’t think my child is at risk for HPV, n (%) Because I don’t want the doctor talking to my child about sex/STIs, n (%) Because if my child gets vaccinated against HPV, he/she might not use condoms when he/she has sex, n (%) Because I don’t want my child to think it’s OK to start having sex if he/she gets this vaccine, n (%) Because I don’t know enough about HPV, I want to talk to my child’s doctor first, n (%) Other reason, n (%)
color subjects’ feelings about it. In the United States, by comparison, the vaccine has been at the center of controversy and negative attention for much of the time since its approval. Conversely, however, U.S. subjects have also been exposed to advertising campaigns touting the benefits of the vaccine. Indeed, the period during which this survey was administered at Bellevue coincided with a widespread print and television advertisement campaign promoting the HPV vaccine. The Salvadoran subjects were more likely than the Bellevue subjects to have a history of abnormal cervical cytology. A desire to spare their daughters this experience could explain their greater acceptance of HPV vaccination. In other studies, experience with an abnormal Pap test was found to make parents more likely to want HPV vaccination for their children.28,29 Additionally, cervical cancer is much more common in El Salvador than it is in the United States. Thus, it may be that upon learning that the HPV vaccine prevents cervical cancer, a disease with which Salvadorans are more likely to have some experience than the Bellevue population, the former are more willing to accept it for their children. This study identified an interesting subgroup in both populations (though more notable in the Bellevue group) that would accept HPV vaccination for themselves but not for their children. In neither Table 4. Attitudes About Vaccines in General by Location of Survey Bellevue N 5 148
El Salvador N 5 160
P Value
Believe that vaccines are important for the health of my child Agree 141 (95.2%) 160 (100%) Neutral 5 (3.4%) 0 (0%) ! 0.0001 Disagree 2 (1.4%) 0 (0%) Concerned that some vaccines are not safe/good for my child Agree 51 (34.4%) 41 (25.6%) Neutral 51 (34.5%) 4 (2.5%) ! 0.0001 Disagree 46 (31.1%) 115 (71.9%) Trust older vaccines more than new vaccines Agree 35(23.6%) 21 (13.1%) Neutral 74 (50.0%) 17 (10.6%) ! 0.0001 Disagree 39 (26.4%) 122 (76.3%)
8 6 0 3
(17.0%) (12.7%) (0%) (6.4%)
7 (14.9%) 20 (42.5%) 3 (6.4%)
El Salvador N 5 20 4 1 0 0
(20.0%) (5.0%) (0%) (0%)
0 (0%) 8 (40.0%) 7 (35.0%)
population can this finding be attributed to younger ages of the subjects, nor can the subgroup be defined by a difference in their concerns about the HPV vaccine. It could be that this subgroup of mothers has younger children than the rest of the study population, but because of the way our data were collected this calculation was not possible. However, it seems unlikely that the subgroup would have significantly younger children than the general study population, given that the average ages of the mothers did not differ. This is an intriguing finding that merits further investigation; it has potential consequences for acceptance of the vaccine. Reasons for objecting to or being unsure about HPV vaccination were for the most part similar in the Bellevue and El Salvador groups, but there were some interesting differences. The reasons that were similar include not knowing enough about HPV, wanting to speak to the child’s health care provider first, and the fact that the vaccine is new. The two groups differed in the levels of their concern about condoning early sexual activity by consenting to the HPV vaccine and in their sense of whether their own children were at risk for HPV. Bellevue parents were more concerned than Salvadorans about condoning early sexual activity. There are many possible explanations for this finding. One is that although both populations are heavily Catholic, they come from different social and cultural contexts that place different values on marrying and having children at a young age. This is an interesting and somewhat counterintuitive finding that merits further investigation. Bellevue subjects were less concerned than Salvadorans that their children were at risk for HPV and cite that as a reason to object to HPV vaccination. A possible explanation for this finding is that Bellevue subjects simply have less experience with HPV and cervical cancer than do Salvadoran subjects and are thus less likely to see it is a threat to their children. Subjects in both groups most commonly objected to HPV vaccination for their children because of their lack of familiarity with HPV. This is consistent with findings in similar studies such as one by Bair and
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colleagues that also looked at HPV vaccine acceptability among Latina mothers.30 This finding highlights the need for educational materials to be made available in waiting rooms or during doctor visits. It is important that any such materials be designed with the educational background and level of prior knowledge of the target population in mind. The two study populations differed in their attitudes toward vaccines in general, though in both populations the vast majority of subjects indicated that their children had received all vaccines offered by health care providers. Salvadoran subjects were more trusting of vaccines and were more likely to feel that vaccines are always good for their children than were the Bellevue subjects. A possible explanation for these findings is the increased suspicion of vaccines in the United States because of the controversy over a possible link between the measles-mumps-rubella vaccine and autism. The suggestion that a vaccine might cause autism may have increased suspicion of all vaccines. Despite the fact that newer research has shown this association to be a false,31 American parents may be scrutinizing vaccines with new eyes. This study has several strengths. An important one is that it provides information about an under-studied group in the U.S. population. Because Latina women still get cervical cancer at higher rates than other women in the United States, an understanding of how the vaccine is being received in that population and what can be done to ensure maximal vaccination rates is important. The study also helps to build support for making the HPV vaccine available in El Salvador by demonstrating that parental acceptance will not be a barrier to widespread vaccination of children there. It also identifies common concerns held by parents about HPV vaccination, many of which are can be addressed by relatively simple interventions. Having this information will be important when evaluating the costeffectiveness of universal vaccination in El Salvador. This study also has several limitations. The first is the small sample size, which was limited by the availability of researchers and by the short amount of time spent in El Salvador. Despite the small sample size, however, the differences between the two populations were large and statistically significant. There may have been an element of selection bias in the recruitment of study participants because all women were seeking medical care for themselves or their children at the time they were approached and thus may have been more predisposed to consent to vaccination than they would have been in a nonmedical setting. However, as previously mentioned, the levels of acceptance obtained in this study are consistent with those reported in similar research. Another limitation of this study is that it compares two groups that are dissimilar except on the issues of cultural background,
language, and religion. Given all the differences between these two populations, several possible confounders, especially education and history of abnormal cytology, could explain the difference in HPV vaccine acceptability. Another limitation is that at Bellevue, the HPV vaccine is available, whereas in El Salvador, the subject is theoretical. Finally, the Bellevue group completed the survey on their own; Salvadoran subjects had the survey administered to them by a researcher, and that could have affected the answers given. It is possible that Salvadorans were more accepting of the vaccine out of the desire to please the researcher or to give the answer they perceived as being the correct one. However, researchers administering the survey in El Salvador made every attempt to limit their personal bias about the vaccine. Both researchers who administered the survey in El Salvador were Spanish-speaking female medical students who were not involved in the medical care being sought by the subjects. The researchers made this fact clear to each woman they approached. Future research on this topic should include more subjects, which would allow for more powerful comparisons. As the vaccine becomes available in developing countries, it will be important to identify any barriers to effective vaccination programs. In El Salvador, parental acceptance is unlikely to be an issue, but for an HPV vaccination program to achieve its potential in that country, identifying other barriers will be critical.
References 1. Centers for Disease Control and Prevention: Genital HPV Infection, CDC Fact Sheet. May 2004. Accessed: http://www.cdc.gov/std/HPV/STDFact-HPV.htm#common, November 2006 2. Ferlay J, Bray F, Pisani P, et al: GLOBOCAN 2002 cancer incidence: Mortality and prevalence worldwide. IARC CancerBase No. 5, version 2.0. Lyon, IARC Press, 2004 3. Ho GY, Bierman R, Beardsley L, et al: Natural history of cervicovaginal papillomavirus infection in young women. N Engl J Med 2002; 347:1645 4. Villa LL, Costa RL, Petta C, et al: Prophylactic quadrivalent human papillomavirus (types 6, 11, 16 and 18) L1 virus-like particle vaccine in young women: A randomized double-blind placebo-controlled multi-center phase II efficacy trial. Lancet 2005; 6:256 5. Youth Risk Behavior Survey 2005. Accessed: http: //www.cdc.gov/mmwr/preview/mmwrhtml/ss5505a1.htm, March 2007. 6. Chan SS, Cheung TH, Lo WK, et al: Women’s attitudes on human papillomavirus vaccination to their daughters. J Adolesc Health 2007; 41:204 7. Constantine NA, Jerman P: Acceptance of human papillomavirus vaccination among Californian parents of daughters: A representative statewide analysis. J Adolesc Health 2007; 40:108
Podolsky et al: HPV Vaccine Acceptability by Latino Parents 8. Davis K, Dickman E, Ferris D, et al: Human papillomavirus vaccine acceptability among parents of 10- to 15-yearold adolescents. J Low Genit Tract Dis 2004; 8:188 9. Olshen E, Woods ER, Austin SB, et al: Parental acceptance of the human papillomavirus vaccine. J Adolesc Health 2005; 37:248 10. Lawson, HW: Cancer of the cervix and other HPV-related cancers: An overview. July 2006. Accessed: www.cdc. gov/vaccines/ed/ciinc/archived/hpv/downloads/2-HPV.ppt, November 2006. 11. Centers for Disease Control and Prevention: Comparing cervical cancer by race and ethnicity. 2003. Accessed: http://www.cdc.gov/cancer/cervical/statistics/race.htm, October 2006. 12. Brewer NT, Fazekas KI: Predictors of HPV vaccine acceptability: A theory-informed, systematic review. Prev Med 2007; 45:1074 13. Ferlay et al: 2004. 14. National Cancer Institute SEER data. Accessed: http://canques.seer.cancer.gov, March 2007. 15. Newmann SJ, Goldberg AB, Aviles R, et al: Predictors of contraception knowledge and use among postpartum adolescents in El Salvador. Am J Obstet Gynecol 2005; 192:1391 16. Centers for Disease Control: Accessed.http://www.cdc.gov/ reproductivehealth/surveys/ElSalvador_LD.htm%23fig2. March 2007. 17. Agurto I, Sandoval J, De La Rosa M, et al: Improving cervical cancer prevention in a developing country. Int J Qual Health Care 2006; 18:8 18. Miniterio de Salud Publica y Asistencia Socia, Direccion de Planificacion de los Servicios de Salud Gerencia de Informacion en Salud: Variables e Indicadores del MSPAS, El Salvador Enero-Diciembre del 2006, El Salvador, Author, 2007. Ministerio de Salud Publica y Asistencia Social, Direccion de Planificacion de los Servicios de Salud Gerencia de Informacion en Salud: Variables e Indicadores del MSPAS, El Salvador, Enero-Diciembre del 2006. Accessed: http://www.mspas.gob.sv/pdf/indicadores_inst/indicadores2006.pdf, March 2007. 19. Sirovich BE, Welch HG: The frequency of Pap smear screening in the United States. J Gen Intern Med 2004; 19:243 20. Agurto I, Sandoval J, De La Rosa M, et al: Improving cervical cancer prevention in a developing country. Int J Qual Health Care 2006; 18:8
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21. Slomovitz BM, Sun CC, Frumovitz M, et al: Are women ready for the HPV vaccine? Gynecol Oncol 2006; 103:151 22. Davis K, Dickman E, Ferris D, et al: Human papillomavirus vaccine acceptability among parents of 10- to 15-yearold adolescents. J Low Genit Tract Dis 2004; 8:188 23. Lazcano-Ponce E, Rivera L, Arillo-Santillan E, et al: Acceptability of a human papillomavirus (HPV) vaccine among mothers of adolescents in Cuernavaca, Mexico. Arch Med Res 2001; 32:243 24. National Breast and Cervical Cancer Early Detection Program 5-Year Summary (2002-2006).Accessed: http: //www.cdc.gov/cancer/NBCCEDP/data/, March 2007. 25. Sirovich BE, Welch HG: The frequency of Pap smear screening in the United States. J Gen Intern Med 2004; 19:243 26. Carey P, Gjerdingen DK: Follow-up of abnormal Papanicolaou smears among women of different races. J Fam Pract 1993; 37:583 27. Breitkopf CR, Pearson HC, Breitkopf DM: Poor knowledge regarding the Pap test among low-income women undergoing routine screening. Perspect Sex Reprod Health 2005; 37:78 28. Dempsey AF, Zimet GD, Davis RL, et al: Factors that are associated with parental acceptance of human papillomavirus vaccines: A randomized intervention study of written information about HPV. Pediatrics 2006; 117: 1486 29. Chan SS, Cheung TH, Lo WK, et al: Women’s attitudes on human papillomavirus vaccination to their daughters. J Adolesc Health 2007; 41:204 30. Davis K, Dickman E, Ferris D, et al: Human papillomavirus vaccine acceptability among parents of 10- to 15-year-old adolescents. J Low Genit Tract Dis 2004; 8:188 31. Chan SS, Cheung TH, Lo WK, et al: Women’s attitudes on human papillomavirus vaccination to their daughters. J Adolesc Health 2007; 41:204 32. Bair RM, Mays RM, Sturm LA, et al: Acceptability of human papillomavirus vaccine among Latina mothers. J Adolesc Health 2006; 40(suppl 1):S16 33. Madsen KM, Hviid A, Vestergaard M, et al: A populationbased study of measles, mumps, rubella vaccination and autism. N Engl J Med 2002; 347:1477
Original Study HPV Vaccine Acceptability by Latino Parents: A Comparison of U.S. and Salvadoran Populations Rebecca Podolsky, BA, Miriam Cremer, MD, MPH, Jessica Atrio, MD, Tsivia Hochman, MS, and Alan A. Arslan, MD New York University School of Medicine, Department of Obstetrics & Gynecology and Department of Biostatistics, New York, NY, USA; Basic Health El Salvador, San Salvador, El Salvador
Abstract. Study Objective: To characterize and compare acceptability of human papillomavirus (HPV) vaccination by Latino parents at an urban medical center in the United States and a community hospital in El Salvador. Design: After reading an information sheet on HPV, 148 subjects at Bellevue Hospital in New York City and 160 subjects at Hospital Nacional de Santa Gertrudis in San Vicente, El Salvador, completed a survey. Results were analyzed using chi-square, Fisher’s exact test, and Student’s t-tests. Results and Conclusions: Parental acceptance of HPV vaccination was higher in a sample of Salvadoran subjects than in a sample of U.S. Latinas (P ! 0.001 for daughters and sons). Reasons for objecting to HPV vaccination differ in the two locations. There are important differences between Salvadoran and U.S. subjects. Salvadorans are more accepting of HPV vaccination, and parental acceptance is unlikely to be a barrier to widespread vaccination in El Salvador. Targeted educational materials are needed in both locations.
Adddress correspondence to: Miriam Cremer, MD, NYU School of Medicine Department of Obstetrics and Gynecology, 550 First Avenue, New York, NY 10016.; E-mail: [email protected]
sexually active adults will be infected with HPV during their lifetimes.2,3 The Food and Drug Administration approved the first multivalent HPV vaccine in 2006. This vaccine prevents acquisition of subtypes 6, 11, 16, and 18, which together cause approximately 90% of genital warts and 70% of cervical cancers.3 In order for this vaccine to be maximally effective clinically, widespread vaccination of HPV-naı¨ve individuals is required. Practically, this means vaccinating children before the onset of sexual activity. According to the 2005 Youth Risk Behavior Survey, 29.3% of females and 39.3% of males in the United States have had sexual intercourse by the time they are in ninth grade.4 Thus, assessing the attitudes of parents about the HPV vaccine is critical because they could constitute a major barrier to successful implementation of widespread HPV vaccination. Several previous studies have looked at the question of acceptability of the HPV vaccine among parents in various populations.5,6,7 In the United States, Latina women are among the least likely to receive regular Papanicolaou (Pap) screenings8 and are among the most likely to be diagnosed with and die of cervical cancer.9 However, there is a dearth of information about acceptability in low-income Latino populations in the United States, even as this is a population that stands to benefit greatly from HPV vaccination.10 There is even less research into how the vaccine will be received in developing countries, where 83% of cervical cancer cases occur.11 In El Salvador, where this survey was administered, in the year 2000 there were 40.6 cases diagnosed per 100,000 women, compared to 8.7 per 100,000 in the United States.12 As in the United States, El Salvador has a high rate of adolescent sexual activity, with 88% of females reporting their first coitus before age 1913 and 100 births per 1000 women aged 15 to 19.14 Thus, widespread vaccination of children will
Ó 2009 North American Society for Pediatric and Adolescent Gynecology Published by Elsevier Inc.
1083-3188/09/$36.00 doi:10.1016/j.jpag.2008.05.010
Key Words. Human papillomavirus (HPV) vaccine— Acceptability—Latino
Introduction Human papillomavirus (HPV), the causative agent in genital warts and cervical carcinoma, is one of the most common sexually transmitted infections in the United States1 and worldwide.2 At least 20 million Americans are currently infected with HPV and nearly half of Sources of Support: Funding came from the NYU School of Medicine’s Department of Obstetrics and Gynecology and from Basic Health El Salvador, a nongovernmental organization dedicated to improving cervical cancer screening and prevention in El Salvador.
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be necessary to ensure maximal effectiveness of the vaccine in El Salvador. Rates of cervical cancer have decreased in the developed world since the successful implementation of widespread Pap screening. In the developing world, such screening is less feasible because of cost and health care infrastructure requirements, so the rates of cervical cancer remain high. The public health system in El Salvador makes Pap tests available, but one study found that insufficient supplies, loss of samples, slow turnaround time, a reading backlog, and poor quality control greatly decreased the efficacy of screening efforts.15 Indeed, the rates of abnormal Pap test results in the United States and El Salvador are nearly equal, but Salvadoran women have a much higher incidence of and mortality rate from cervical cancer.16,17 This fact highlights the apparent failure of current screening methods in that country, including Pap tests. Thus the HPV vaccine has great potential to decrease the incidence of cervical cancer in countries like El Salvador. An improved understanding of how the Salvadoran population will receive this vaccine is critical to ensuring that when the vaccine becomes available in that country, it can be maximally effective. This study offers a comparison between two economically disadvantaged Latino populations, one of which has access to the HPV vaccine and one of which does not. Subjects at both sites can safely be described as economically disadvantaged by virtue of their having sought care at our two recruitment sites. Bellevue is a municipal hospital whose patients are either uninsured or insured by state or federal insurance programs designed to cover low-income families. Subjects recruited at the Hospital Nacional de Santa Gertrudis in El Salvador came from the surrounding semirural and rural areas where an estimated 50% of Salvadorans live in poverty and close to 25% live in extreme poverty. Of the country’s approximately 6,000,000 inhabitants, as of 2002, 80%were covered by the public health system.18 The goals of this study were to characterize levels of parental acceptance of HPV vaccination for children aged 8 to 18 in these two populations and to assess parents’ reasons for refusing HPV vaccination for their children. The two study populations share a common language and religious background and, to some degree, a cultural background.* The purpose of comparing these two populations is to provide insight into the potential impact of differences such as vaccine availability, media attention, attitudes about vaccines in general, and knowledge about HPV and vaccine acceptability. Materials and Methods Mothers of children between the ages of 8 and 18 were approached in the waiting rooms of the Bellevue
Hospital pediatric clinic in New York City and the Hospital Nacional de Santa Gertrudis (HNSG) in San Vicente, El Salvador. Potential subjects were asked the ages of their children and whether they would be willing to complete a survey about the HPV vaccine. Eligibility criteria were slightly different at the two sites because of the low level of literacy in the Salvadoran community. At both sites, subjects had to be at least 18 years old and the parent or guardian of a child between the ages of 8 and 18. At Bellevue, subjects had to be able to read and write either English or Spanish because the survey was self-administered there, whereas at HNSG, literacy was not a requirement; a researcher administered the survey. No compensation was provided for participation in the survey at either site. It is certainly possible that there were potential subjects in the Bellevue population who could not read and write. The ability to read and write was an inclusion criterion at this site, so these people may have been among the small number of refusals. Researchers did not press those who declined to participate about their reasons for refusing. The research instrument consisted of a 10-item fact sheet about HPV (Fig. 1) that was developed by the research team and an anonymous, 28-item survey (Fig. 2). Many of the questions in the survey (10 and 20 through 28) were taken or adapted from a questionnaire developed at the University of Texas.19 The survey was translated into Spanish by fluent speakers of the language with the help of a Salvadoran physician involved in the study. Question 15, which asks about taking the advice of the doctor about vaccines, and question16, which asks about vaccination requirements, were omitted by researchers when administering the survey in El Salvador. Nationwide vaccination campaigns are carried out several times each year there, but the vaccines are not usually administered by doctors, and requirements do not exist as they do in the United Stares. It was believed that Salvadoran subjects would not be able to answer these questions appropriately. This study was approved by the Institutional Review Board at the New York University School of Medicine and by the Ministry of Health in El Salvador. We hypothesized that acceptance would differ in the two study populations. Based on the literature, we estimated a 70% parental acceptance rate of HPV vaccination for daughters in the Bellevue group and an 85% acceptance rate in the HNSG group. We based our hypothesis on the results of two studies: one by Davis and colleagues20 that looked at parental acceptance in a U.S. population before and after an intervention that consisted of a fact sheet about HPV; and the other by Lazcano-Ponce and colleagues that looked at acceptance among mothers in Cuernavaca, Mexico.21 We estimated a sample size of 134 per group to detect a difference of 15% between the two groups based on
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Facts about Human Papillomavirus (HPV) 1. HPV is spread by sexual activity. 2. HPV is very common (at least 50 in their lives).
of people who have sex will have HPV at some point
3. Most people who have HPV don’t know they have it. 4. There are many kinds of HPV and not all of them cause health problems. 5. Only some kinds of HPV cause health problems like genital warts or cervical cancer. 6. Most women who have HPV will NOT develop cervical cancer, and will likely get rid of the virus on their own without medical treatment. 7. Condoms do not always protect against the spread of HPV. 8. You can get HPV without having sexual intercourse (penetration sex); it is transmitted by genital -to-genital co ntact, not by the exchange of bodily fluids. 9. There is no cure for HPV, but there are treatments for problems such as genital warts and cervical cancer that are caused by HPV. There is a new vaccine against the kinds of HPV that most often cause cervical cancer and genital warts. This vaccine is most effective if given before a person becomes sexually active. The HPV vaccine is now available for girls age nine and older.
Figure 1. Fact Sheet Read by Subjects Prior to Completing Questionnaire
80% power and an alpha level of 0.05. Descriptive statistics were calculated on all survey items. Subgroups within the study population were compared using chi-square, Fisher’s exact test, and Student’s t-tests. Results Of the Salvadoran women at Hospital Nacional de Santa Gertrudis, 188 were asked to participate in the study. Of these, 9 (4.7%) refused, and 19 (10.1%) were ineligible. The number of women who completed the survey was 160. At Bellevue, a total of 229 people were approached as potential participants. Of these, 17 (7.4%) refused, and 12 (5.2%) were ineligible. Ultimately, 200 people completed the survey, 153 of whom (76.5%) were Latino. For the purposes of this study, we chose to include only Latino subjects. Additionally, 5 of the 153 Latino Bellevue subjects were male. We chose to exclude them from the analysis. Therefore, the Bellevue group contained 148 subjects. Demographic data for both groups are listed and compared in Table 1. In summary, Salvadorans were much less familiar with HPV and the HPV vaccine than were Bellevue subjects. Of the Salvadoran subjects, 70% indicated that they had never heard of HPV or the vaccine before reviewing the fact sheet accompanying this survey, compared to 12.2% of Bellevue subjects (P ! 0.0001). The Salvadoran study population had lower levels of education than did the Bellevue group. Most notably, 18.8% of
Salvadoran study subjects had never been to school; none of the Bellevue subjects fell into this category. Of the Bellevue subjects, 46.6% were graduates of high school or higher education; 11.9% of Salvadoran subjects were in that category (chi-square 45.48, P ! 0.001). Salvadoran subjects had a higher mean number of children than did Bellevue subjects (4.0 vs. 2.4, t 5 9.65, P ! 0.001), and their children were older than the children of Bellevue subjects (14.2 years vs. 12.7 years, P ! 0.02). Bellevue subjects were more likely to report having had a gynecologic exam within the past 1 to 2 years than were Salvadoran subjects (92.6% vs. 62.5%, P ! 0.0001). Despite this discrepancy, Salvadoran subjects were approximately twice as likely as Bellevue subjects to report a history of abnormal cytology (33.8% vs. 16.3%, chi-square 5 12.35, P 5 0.002), although some of the abnormal test results reported by subjects in both groups may have been due to inflammation or infection. Data from both El Salvador and the United States that measured rates of abnormal Pap tests on the basis of cytologic diagnosis yielded much lower incidences than did data based on patient self-report. Data from the Salvadoran Ministry of Health indicate that in 2005, 3.5% of Pap tests done in that country were read as abnormal. Studies based on pathology results done in the United States cite rates of abnormal cervical cytology between 3% and 10%, depending on the study population.22 Despite this, one nationwide study done in the United States in 2004 found that 20% of women surveyed reported at least
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HPV Vaccine Survey 1. Please mark one answer: __I understood everything I just read about HPV and the HPV vaccine…………..1 __I understood some of what I just read about HPV and the HPV vaccine………..2 __I understood very little of what I just read about HPV and the HPV vaccine…..3 __I did not understand what I just read about HPV and the HPV vaccine……….4 2. Please mark one answer: __I already knew all of what I just read about HPV and the HPV vaccine………..1 __I already knew some of what I just read about HPV and the HPV vaccine…….2 __I have heard of HPV but didn’t know very much of what I just read…………3 __I have never heard of HPV before reading the information sheet……………..4 Demographic Information: 3. Are you:
__Female…………………………………………………………..1 __Male…………………………………………………………….2
4. How old are you?
________
5. Race (mark one answer): __Hispanic…………………………………………………………………1 __White/Caucasian………………………………………………………..2 __Black/African American………………………………………………..3 __Asian/Pacific Islander…………………………………………………..4 __Native American/Aleutian Eskimo……………………………………..5 __Other (_________________________)………………………………..6 6. What language do you usually speak at home? __English………………………………………………………………….1 __Spanish………………………………………………………………….2 __Chinese………………………………………………………………….3 __Korean…………………………………………………………………..4 __Russian……………………………………………………………….…5 __French…………………………………………………………………..6 __Bengali………………………………………………………………….7 __Tagalog…………………………………………………………………8 __Polish…………………………………………………………………...9 __Hindi……………………………………………………………………10 __Urdu…………………………………………………………………….11 __Other language (______________________________________)…….12 7. Religion (mark one answer): __Catholic…………………………………………………………………1 __Protestant……………………………………………………………….2 __Jewish………………………………………………………………….. 3 __Muslim………………………………………………………………….4 __Hindu…………………………………………………………………...5 __Jehovah’s Witness……………………………………………………...6 __No religion……………………………………………………………...7 __Other (___________________________)……………………………..8
Figure 2. H2PV Vaccine Survey
one abnormal Pap test result.23,24 The discrepancy between subject self-report and data based on cytology may be a result of the lack of understanding among women of the purpose of Pap screening and of the various components of a gynecological exam.25
Acceptance of HPV vaccination for sons, daughters, and oneself differs in the two study populations (Table 2). It is notable that in both groups, but more strikingly in the Bellevue population, more subjects would accept vaccination for themselves than for either their sons or
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8. What is your highest level of education? __Elementary School………………………………………………1 __Some high school………………………………………………..2 __High school graduate/GED……………………………………...3 __Associate’s Degree………………………………………………4 __Some college…………………………………………………….5 __College Graduate……………………………………………….. 6 __Graduate School…………………………………………………7 9. How many children do you have? Age/sex of children (Fill in age and circle sex) _____
male…1
female…2
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male…1
female…2
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male…1
female…2
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male…1
female…2
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male…1
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10. Did your children receive all vaccinations that were offered by their doctor/nurse? (mark one answer) __Yes…1_ _No…2 __I don’t know…3
11. If your child has not received all of his/her vaccines, why not? (choose one) __We were living in another country……………………1 __We couldn’t come to doctor/didn’t have a doctor…….2 __I was concerned about side effects……………………3 __I didn’t think my child would get the disease…………4 __I believed the disease was not serious…………………5 __I was concerned about the cost of the shot…………….6 __Other reason (Specify_______________________)…..7 12. Did your children experience any side effects or problems with any vaccinations? (mark one answer) __Yes…1 __No…2 __I don’t know…3 If yes, please describe:____________________________________________________ _ Please circle the answer choice that best describes your feelings about the question. 13. I believe vaccines are important to the health of my child. Strongly Agree…1 Agree…2 Neutral…3 Disagree…4
Strongly Disagree…5
Figure 2. (Continued)
their daughters. At Bellevue, 78.4% of subjects would accept the HPV vaccine for themselves, whereas 68.2% and 58.7% would consent to HPV vaccination for their daughters and sons, respectively. Of the Bellevue subjects, 16.2% said they would accept the vaccine for themselves but were unsure about or would refuse vaccination for their daughters. Only 3.75% of Salvadoran subjects responded this way. The average age
among the subgroup at Bellevue was 37.12 years, and in El Salvador 38.5 years, compared to 37.5 years and 39.2 years in the Bellevue and Salvadoran populations, respectively. The reasons given for being unsure about or refusing HPV vaccination for one’s daughters also reflected the reasons most commonly given by the study population as a whole. These reasons are discussed later.
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Podolsky et al: HPV Vaccine Acceptability by Latino Parents 14. I am concerned that some vaccines are not safe/not good for my child. Strongly Agree…1 Agree…2 Neutral…3 Disagree…4 Strongly Disagree…5 15. I always take the advice of my child’s doctor about vaccines. Strongly Agree…1 Agree…2 Neutral…3 Disagree…4 Strongly Disagree…5 16. I don’t like immunization requirements because parents know what is best for their child. Strongly Agree…1 Agree…2 Neutral…3 Disagree…4 Strongly Disagree…5 17. I trust older vaccines more than I trust new vaccines . Strongly Agree…1 Agree…2 Neutral…3 Disagree…4
Strongly Disagree…5
18. For women only: Do you have a gynecologic exam performed every 1-2 years? (mark one answer) __Yes…1 __No…2_ _I don’t know…3
19. If no, why not? (Choose one) __Don’t think I need them every year………………………………….1 __Don’t have health insurance…………………………………………2 __Don’t want to go to the doctor that often……………………………3 __Other (please describe________________________________)……4 20. Have you ever had an abnormal PAP (Papanicolaou) test/smear? (mark one answer) _Yes…1 __No…2 __I don’t know…3 21. Have you ever had colposcopy? (a procedure that your doctor uses to find the cause of a Pap smear abnormality.) (mark one answer) _Yes…1 __No…2 __I don’t know…3 22. Have you ever had a hysterectomy (surgery to remove the uterus or “womb”? (mark one answer) _Yes…1 __No…2 __I don’t know…3 23. If the HPV vaccine were to work at any age, would you get the vaccine for yourself? (mark one answer) _Yes…1 __No…2 __I don’t know…3 24. If you marked “No,” why not? __Because it is a new vaccine………………………….………….…..……1 __Because I don’t think I am at risk for HPV………………………....…...2 __Because I don’t know enough about HPV/I want to talk about the vaccine with my doctor first………………….…….…..…..3 __Another reason..(Please state reason:_______________________)…......4 If you have a daughter between the ages of 8 and 18, please answer questions 25 and 26. If you do not have a daughter in this age group, please skip to question 27. 25. Would you give consent for your daughter to receive the HPV vaccine? (mark one answer) _Yes…1_ _No…2 __I don’t know…3
Figure 2. (Continued)
Subjects who responded that they were unsure or that they would refuse HPV vaccination for their child or children were asked about their reasons for doing so (Table 3). In both groups, the most commonly chosen reason from a list of possible choices was ‘‘Because I don’t know enough about HPV. I want to talk to my child’s doctor first’’ (42.5% at Bellevue; 40% in El Salvador). A smaller group in each location
expressed concern about the HPV vaccine’s being new (17% at Bellevue; 20% in El Salvador). Subjects at Bellevue were more likely than their Salvadoran counterparts to express the concern that consenting to HPV vaccination would be interpreted as tacit approval of early sexual activity (14.9% vs. 0%). Bellevue subjects were also more likely to feel that their children were not at risk for HPV (12.7% vs. 5%).
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26. If you marked“No,” or“I don’t know,” why not? __Because it is a new vaccine ………………………… .………….…..……1 __Because I don’t think my daughter is at risk for HPV……………....2 __Because I don’t want the doctor talking to my daughter about sex/sexually transmitted infections……….……………………...……3 __Because if my daughter gets vaccinated against HPV, she might not use condoms when she has sex……………………… 4 __Because I don’t want my daughter to think it’s ok to start having sex if she gets this vaccine ………………………………………….…5 __Because I don’t know enough about HPV, I want to talk about the vaccine with my child’s doctor first………….…….…..…..6 __Another reason..(Please state reason:_______________________)…......7
If you have a son between the ages of 8 and 18, please answer questions 27 and 28. 27. Would you give consent for your son to receive the HPV vaccine? (mark one answer) __Yes…1 __No…2 __I don’t know…3 28. If you marked “No,” or “I don’t know,” why not? __Because it is a new vaccine ………………………….………….…..……1 __Because I don’t think my son is at risk for HPV………………….....2 __Because I don’t want the doctor talking to my son about sex/sexually transmitted infections ……….……………………...……3 __Because if my son gets vaccinated against HPV, he might not use condoms when he has sex……………..…………4 __Because I don’t want my son to think it’s ok to start having sex if he gets this vaccine………………….……………………….5 __Because I don’t know enough about HPV, I want to talk about the vaccine with my child’s doctor first………….………..….6 __Another reason..(Please state reason:_______________________)…....7 Thank you for your help!!
Figure 2. (Continued)
Attitudes about vaccines in general differ significantly in these two populations (Table 4). Of Salvadoran subjects, 72%, and of Bellevue subjects, only 31% disagreed with the statement ‘‘Some vaccines are not safe/not good for my child.’’ Subjects at Bellevue were more likely than were Salvadoran subjects to agree or feel neutral about the statement ‘‘I trust older vaccines more than new vaccines’’. At Bellevue, 24% of subjects agreed with the previous statement, 50% felt neutral, and 26% disagreed. In El Salvador, 13% agreed, 11% felt neutral, and 76% disagreed; most of those who disagreed indicated to the researchers that they trusted new vaccines more than older ones. Discussion Based on the results of this study, several conclusions can be drawn. First, parental acceptance of HPV vaccination is higher in El Salvador than in the United States. This finding supports both our initial hypothesis and the findings of similar studies looking at acceptance of HPV vaccination in the United States
and in developing countries. Second, there are some interesting differences in the reasons given for objecting to HPV vaccination for one’s children. Finally, attitudes about vaccines in general differ between the two study populations. There are many possible reasons for the different levels of acceptance of the HPV vaccine in the two populations: difference in the demographics of the two populations, a higher rate of abnormal cytology among Salvadoran women, the fact that the HPV vaccine is available to the Bellevue population and has not yet been approved in El Salvador, and a difference in the level of prior knowledge of HPV in the two populations. Salvadoran subjects tend to be less educated and less familiar with HPV than Bellevue subjects. As education campaigns about HPV and the HPV vaccine target the Salvadoran population, acceptance of the vaccine may change. Several studies have looked at the impact on acceptance of the HPV vaccine of providing information about HPV and the vaccine, and the results have been equivocal. One study, by
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Table 1. Demographic Characteristics of Participants on the Basis of Location of Survey Bellevue N 5 148
Characteristic
El Salvador N 5 160
Age (years), mean (SD) 37.5 (6.8) Familiarity with HPV and the HPV vaccine, n (%) Already knew everything on fact sheet 14 (9.5%) Already knew some of fact sheet 62 (41.9%) Had heard of HPV but did not know very much 54 (36.5%) Never heard of HPV before fact sheet 18 (12.2%) Highest level of education, n (%) No school 0 (0%) Elementary school 38 (25.7%) Some high school 41 (27.7%) High school/GED 42 (28.4%) Associate’s degree 7 (4.7%) Some college 11 (7.4%) College 8 (5.4%) Postgraduate 1 (0.7%) Proportion of high school graduates, n (%) Did not complete high school 79 (53.4%) Graduated from high school 69 (46.6%) Total number of children, mean (SD) 2.4 (1.1) Age of subjects’ children, mean (SD) 12.7 (5.5) Subject has had a gynecologic exam in the past 1-2 years Yes 137 (92.6%) No 9 (6.1%) Don’t know 2 (1.4%) Subject has history of abnormal PAP, n (%) Yes 24 (16.3%) No 116 (78.9%) Don’t know 7 (4.8%) Missing 1 (0.7%) Subject’s children have received all vaccines, n (%) Yes 144 (97.3%) No 3 (2.0%) Don’t know 1 (0.7%)
Dempsey and colleagues, found no significant increase in acceptance of HPV vaccination after the introduction of a fact sheet, despite the increased knowledge about HPV.26 However, another study, by Chan and colleagues, which also looked at parental acceptance of HPV vaccination before and after an information-based intervention, did find a statistically significant increase in acceptance of vaccination.27 Thus, from the literature it is difficult to predict what effect increasing knowledge will have on Salvadorans’ acceptance of HPV vaccination.
Statistical Test and Value
P Value
39.2 (7.4)
t value 5 2.06
0.040
4 (2.5%) 13 (8.1%) 31 (19.4%) 112 (70.0%)
N/A
! 0.0001
30 (18.8%) 95 (59.4%) 16 (10.6%) 6 (3.1%) 1 (0.6%) 1 (0.6%) 0 (0%)
N/A
! 0.0001
141 (88.1%) 19 (11.9%) 4.0 (1.9) 14.2 (5.4)
Chi-square 5 45.48
! 0.001
t value 5 9.65 N/A
! 0.0001 ! 0.02
100 (62.5%) 59 (36.9%) 1 (0.6%)
N/A
! 0.0001
54 (33.8%) 99 (61.9%) 7 (4.4%) 0 (0%)
Chi-square 5 12.35
0.002
149 (93.1%) 10 (6.3%) 1 (0.6%)
N/A
0.17
The HPV vaccine has not yet been approved in El Salvador, so it was not available when the subjects participated in this study. Bellevue Hospital had just obtained the vaccine when this study began enrollment, so it was available there. Salvadoran subjects were answering questions about a theoretical vaccine, so they may have been more focused on its benefits, whereas the Bellevue subjects were facing a more immediate and real decision. Because the vaccine is not yet available in El Salvador, no attention has been paid to the vaccine, positive or negative, that might
Table 2. Acceptance or Refusal of HPV Vaccination for Survey Participants and for Their Children by Location of Survey Bellevue (N 5 148) Yes
No
Self, n (%) 116 (78.4%) 13 (8.8%) Daughter 8-18 years old, n (%) 101 (68.2%) 14 (9.5%) Son 8-18 years old, n (%) * 27 (58.7%) 8 (17.4%)
I don’t know 19 (12.8%) 33 (22.3%) 11 (23.9%)
El Salvador (N 5 160) Yes
No
141 (88.1%) 5 (3.1%) 140 (87.5%) 7 (4.4%) 9 (87.6%) 3 (2.9%)
Chi-square P Value
I don’t know 14 (8.8%) 13 (8.1%) 10 (9.5%)
6.29 16.90 N/A
0.043 !0.001 !0.001
*Note: Having a son 8-18 was not an eligibility criterion, and only women with sons in this age group answered questions about HPV vaccination for boys. Thus, the number in this group is lower than the number in the total study group.
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Table 3. Reasons for Refusing or Being Unsure About Consenting to HPV Vaccination for Daughter by Location of Survey Bellevue N 5 47
Reason Because it is a new vaccine, n (%) Because I don’t think my child is at risk for HPV, n (%) Because I don’t want the doctor talking to my child about sex/STIs, n (%) Because if my child gets vaccinated against HPV, he/she might not use condoms when he/she has sex, n (%) Because I don’t want my child to think it’s OK to start having sex if he/she gets this vaccine, n (%) Because I don’t know enough about HPV, I want to talk to my child’s doctor first, n (%) Other reason, n (%)
color subjects’ feelings about it. In the United States, by comparison, the vaccine has been at the center of controversy and negative attention for much of the time since its approval. Conversely, however, U.S. subjects have also been exposed to advertising campaigns touting the benefits of the vaccine. Indeed, the period during which this survey was administered at Bellevue coincided with a widespread print and television advertisement campaign promoting the HPV vaccine. The Salvadoran subjects were more likely than the Bellevue subjects to have a history of abnormal cervical cytology. A desire to spare their daughters this experience could explain their greater acceptance of HPV vaccination. In other studies, experience with an abnormal Pap test was found to make parents more likely to want HPV vaccination for their children.28,29 Additionally, cervical cancer is much more common in El Salvador than it is in the United States. Thus, it may be that upon learning that the HPV vaccine prevents cervical cancer, a disease with which Salvadorans are more likely to have some experience than the Bellevue population, the former are more willing to accept it for their children. This study identified an interesting subgroup in both populations (though more notable in the Bellevue group) that would accept HPV vaccination for themselves but not for their children. In neither Table 4. Attitudes About Vaccines in General by Location of Survey Bellevue N 5 148
El Salvador N 5 160
P Value
Believe that vaccines are important for the health of my child Agree 141 (95.2%) 160 (100%) Neutral 5 (3.4%) 0 (0%) ! 0.0001 Disagree 2 (1.4%) 0 (0%) Concerned that some vaccines are not safe/good for my child Agree 51 (34.4%) 41 (25.6%) Neutral 51 (34.5%) 4 (2.5%) ! 0.0001 Disagree 46 (31.1%) 115 (71.9%) Trust older vaccines more than new vaccines Agree 35(23.6%) 21 (13.1%) Neutral 74 (50.0%) 17 (10.6%) ! 0.0001 Disagree 39 (26.4%) 122 (76.3%)
8 6 0 3
(17.0%) (12.7%) (0%) (6.4%)
7 (14.9%) 20 (42.5%) 3 (6.4%)
El Salvador N 5 20 4 1 0 0
(20.0%) (5.0%) (0%) (0%)
0 (0%) 8 (40.0%) 7 (35.0%)
population can this finding be attributed to younger ages of the subjects, nor can the subgroup be defined by a difference in their concerns about the HPV vaccine. It could be that this subgroup of mothers has younger children than the rest of the study population, but because of the way our data were collected this calculation was not possible. However, it seems unlikely that the subgroup would have significantly younger children than the general study population, given that the average ages of the mothers did not differ. This is an intriguing finding that merits further investigation; it has potential consequences for acceptance of the vaccine. Reasons for objecting to or being unsure about HPV vaccination were for the most part similar in the Bellevue and El Salvador groups, but there were some interesting differences. The reasons that were similar include not knowing enough about HPV, wanting to speak to the child’s health care provider first, and the fact that the vaccine is new. The two groups differed in the levels of their concern about condoning early sexual activity by consenting to the HPV vaccine and in their sense of whether their own children were at risk for HPV. Bellevue parents were more concerned than Salvadorans about condoning early sexual activity. There are many possible explanations for this finding. One is that although both populations are heavily Catholic, they come from different social and cultural contexts that place different values on marrying and having children at a young age. This is an interesting and somewhat counterintuitive finding that merits further investigation. Bellevue subjects were less concerned than Salvadorans that their children were at risk for HPV and cite that as a reason to object to HPV vaccination. A possible explanation for this finding is that Bellevue subjects simply have less experience with HPV and cervical cancer than do Salvadoran subjects and are thus less likely to see it is a threat to their children. Subjects in both groups most commonly objected to HPV vaccination for their children because of their lack of familiarity with HPV. This is consistent with findings in similar studies such as one by Bair and
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colleagues that also looked at HPV vaccine acceptability among Latina mothers.30 This finding highlights the need for educational materials to be made available in waiting rooms or during doctor visits. It is important that any such materials be designed with the educational background and level of prior knowledge of the target population in mind. The two study populations differed in their attitudes toward vaccines in general, though in both populations the vast majority of subjects indicated that their children had received all vaccines offered by health care providers. Salvadoran subjects were more trusting of vaccines and were more likely to feel that vaccines are always good for their children than were the Bellevue subjects. A possible explanation for these findings is the increased suspicion of vaccines in the United States because of the controversy over a possible link between the measles-mumps-rubella vaccine and autism. The suggestion that a vaccine might cause autism may have increased suspicion of all vaccines. Despite the fact that newer research has shown this association to be a false,31 American parents may be scrutinizing vaccines with new eyes. This study has several strengths. An important one is that it provides information about an under-studied group in the U.S. population. Because Latina women still get cervical cancer at higher rates than other women in the United States, an understanding of how the vaccine is being received in that population and what can be done to ensure maximal vaccination rates is important. The study also helps to build support for making the HPV vaccine available in El Salvador by demonstrating that parental acceptance will not be a barrier to widespread vaccination of children there. It also identifies common concerns held by parents about HPV vaccination, many of which are can be addressed by relatively simple interventions. Having this information will be important when evaluating the costeffectiveness of universal vaccination in El Salvador. This study also has several limitations. The first is the small sample size, which was limited by the availability of researchers and by the short amount of time spent in El Salvador. Despite the small sample size, however, the differences between the two populations were large and statistically significant. There may have been an element of selection bias in the recruitment of study participants because all women were seeking medical care for themselves or their children at the time they were approached and thus may have been more predisposed to consent to vaccination than they would have been in a nonmedical setting. However, as previously mentioned, the levels of acceptance obtained in this study are consistent with those reported in similar research. Another limitation of this study is that it compares two groups that are dissimilar except on the issues of cultural background,
language, and religion. Given all the differences between these two populations, several possible confounders, especially education and history of abnormal cytology, could explain the difference in HPV vaccine acceptability. Another limitation is that at Bellevue, the HPV vaccine is available, whereas in El Salvador, the subject is theoretical. Finally, the Bellevue group completed the survey on their own; Salvadoran subjects had the survey administered to them by a researcher, and that could have affected the answers given. It is possible that Salvadorans were more accepting of the vaccine out of the desire to please the researcher or to give the answer they perceived as being the correct one. However, researchers administering the survey in El Salvador made every attempt to limit their personal bias about the vaccine. Both researchers who administered the survey in El Salvador were Spanish-speaking female medical students who were not involved in the medical care being sought by the subjects. The researchers made this fact clear to each woman they approached. Future research on this topic should include more subjects, which would allow for more powerful comparisons. As the vaccine becomes available in developing countries, it will be important to identify any barriers to effective vaccination programs. In El Salvador, parental acceptance is unlikely to be an issue, but for an HPV vaccination program to achieve its potential in that country, identifying other barriers will be critical.
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