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Barriers to Human Papillomavirus Vaccine Acceptability in Israel
Vaccine 31S (2013) I53–I57
Contents lists available at ScienceDirect
Vaccine journal homepage: www.elsevier.com/locate/vaccine
Review
Barriers to Human Papillomavirus Vaccine Acceptability in Israel William A. Fisher a , Hila Laniado b , Hila Shoval c , Marwan Hakim d,e , Jacob Bornstein e,f,∗ a
Department of Psychology and Department of Obstetrics and Gynecology, University of Western Ontario, London Ontario, Canada Department of Psychology, Tel Aviv University, Tel Aviv, Israel c Medical Scientific Liaison, M.S.D., Israel d The Nazareth Hospital, Nazareth, Israel e Bar-Ilan University Galilee Faculty of Medicine, Nahariya, Israel f Department of Obstetrics and Gynecology, Western Galilee Hospital, Nahariya, Israel b
a r t i c l e
i n f o
Article history: Received 1 February 2012 Received in revised form 6 June 2012 Accepted 18 June 2013 Keywords: Israel HPV vaccine acceptability HPV Cervical cancer Circumcision Attitudes Social support
a b s t r a c t Barriers to human papillomavirus (HPV) vaccine acceptability in Israel include Israel’s relatively low incidence of cervical cancer; the religiously-based 80% circumcision rate in Israel, which is regarded as contributing to the lower incidence of HPV infection in the country; the fact that HPV vaccine provides immunity against only few virus types; the vaccine’s high cost; and the perception that HPV transmission is associated with unacceptable sexual relations. A recent survey has demonstrated that, following media two campaigns, Israeli’s level of awareness of the vaccine increased but the actual vaccination rate remained low, at approximately 10%. Survey findings also indicated that an enduring barrier to HPV vaccination is the vaccine’s high cost. Recent research on a convenience sample of Israeli undergraduate women 21 to 24 years of age showed that intentions to receive HPV vaccination in the coming year were a function of women’s attitudes towards getting vaccinated and their perceptions of social support for doing so. Undergraduate women who intended to be vaccinated perceived the prevention of cervical cancer, avoidance of personal health threat, and avoidance of HPV infection per se to be the advantages of undergoing HPV vaccination. Disadvantages of getting vaccinated included fear of vaccine side effects, cost of the vaccine, and newness of the vaccine, doubts about vaccines, time required to undergo multiple vaccinations, and dislike of injections. Friends’, mothers’ and physicians’ recommendations influenced women’s intentions to be vaccinated in the coming year as well. This article forms part of a regional report entitled “Comprehensive Control of HPV Infections and Related Diseases in Israel” Vaccine Volume 31, Supplement 8, 2013. Updates of the progress in the field are presented in a separate monograph entitled “Comprehensive Control of HPV Infections and Related Diseases” Vaccine Volume 30, Supplement 5, 2012. © 2013 Elsevier Ltd. All rights reserved.
1. Introduction There are some 2.47 million women aged 15 years and older in Israel and estimates for 2008 indicated that approximately 222 women were diagnosed with cervical cancer and about 98 women died from the disease each year [1,2]. By 2025, Israel is projected to experience 302 new cervical cancer cases and 141 cervical cancer deaths per year [1,2]. In addition to cervical cancer, human papillomavirus (HPV) contributes to a portion of Israel’s vulvar, vaginal, and anal cancer cases (Table 1) [1–3]. HPV types 6 and 11 are also the dominant cause of HPV related genital warts in Israel [3]. A recent retrospective study revealed that the annual occurrence of genital warts in Israel is about 17,430 cases [4].
∗ Corresponding author. Tel.: +972 4 9107720; fax: +972 4 9107472. E-mail address: [email protected] (J. Bornstein). 0264-410X/$ – see front matter © 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.vaccine.2013.06.107
The two HPV vaccines currently approved for use in Israel include a bivalent vaccine to protect against HPV 16 and 18 infection (Cervarix® , GlaxoSmithKline Biologicals, Rixensart, Belgium) and a quadrivalent vaccine against HPV 6, 11, 16, and18 infection (Gardasil® , Merck & Co., Whitehouse Station, NJ, USA). The vaccines appear to provide some cross-protection against other HPV types, especially against HPV 31 (both vaccines), 33 and 45 (bivalent vaccine), which are phylogenetically related to HPV 16 and 18. The two vaccines are accessible in the private market and are partially covered by supplementary health insurance policies. To promote vaccine uptake, the Advisory Committee on Immunization Practices (ACIP) in the United States recommended universal vaccination of all 11–12 year-old girls as part of routine preventive care visits, and comprehensive “catch-up” vaccination of adolescent and young adult women between the ages of 13 and 26 years [5]. Despite ACIP recommendation, vaccination coverage rates in the United States remain low: in 2010, 47.7% of 13–17 yearold girls had received one or more doses of HPV vaccine. Of those
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W.A. Fisher et al. / Vaccine 31S (2013) I53–I57
Table 1 Annual incidence of HPV-related anogenital cancers and HPV attributable cases in Israel. Cancer type Cervical Vulvar Vaginal Anal Total
Number of new cases per year 222a 48b 12b 20b 302
% HPV-attributable 100c 43c 70c 88c 89d
Number of annual cases attributed to HPV 222 21 8 18 269
a
Estimated incidence cases for 2008. GLOBOCAN 2008 [1]. Estimated incidence cases for the period 1998-2002 [2]. c HPV-attributable fraction from Forman D et al. [3]. d Calculated as the total number of annual cases attributed to HPV divided by the total number of anogenital cases per year. b
who had received one dose and were eligible to complete the series, 73.2% received all three doses [6–9]. In Israel, private vaccination coverage rates remain low, at around 10% of eligible women. The Israeli Pediatrics Infectious Disease Society and the Israel Association of Obstetrics and Gynecology have published position papers supportive of HPV vaccination [10]. The Israeli national vaccination committee recommended introduction of HPV vaccination as part of the national immunization program and it will be introduced free of charge to the school-based vaccine program in September 2013. The objective of the current paper is to review barriers to HPV vaccination and report on a preliminary study of factors that influence HPV vaccine acceptability in Israel. 2. Barriers to HPV vaccination in Israel A number of barriers to HPV vaccination appear to work against vaccine acceptance in Israel. Without widespread acceptance, vaccination programs cannot take place, herd immunity to HPV will not occur, and HPV infection and sequelae of infection will persist. The following factors are society/individual issues that appear to work against HPV vaccine acceptance in Israel: • There is a relatively low incidence of cervical cancer in Israel (Bornstein J and Shavit O, Vaccine, 2013 [11] and Shavit O et al., Vaccine, 2013 [2]). • Current HPV vaccines are perceived to induce immunity to only a limited number of HPV types. • HPV vaccines are costly in Israel [12]. • The belief that HPV transmission and by extension HPV vaccination are closely associated with unacceptable sexual relations. The Israeli Ministry of Health approved HPV vaccination in 2007 and it will be introduced to the school-based immunization program for 13 year-old girls in September 2013. Until then, the burden of cost was left on the patients, who faced the challenge of covering the high cost of vaccination. The cost of HPV vaccine coverage in Israel currently is equivalent to $800 in the private market, while the average monthly wage is $2,000 [11]; thus, it is quite difficult to finance personal or programmatic vaccination in Israel, especially for the financially disadvantaged, who would have to pay up to $400 for the vaccine even with supplementary health insurance coverage. As HPV vaccination becomes part of Israel’s national school-based immunization program, a decrease in the burden of HPV-related disease is expected within the vaccinated cohort and, in time and via herd immunity, in the wider Israeli population. In the past, before the cost of the vaccine went down, the cost of supporting a national school-based vaccine program had been a main factor in the Israel Ministry of Health’s decision to decline funding of a national HPV vaccination program [13]. At the present
time, a number of additional factors appear to have contributed to resistance to the addition of HPV vaccine in Israel’s national immunization program. Critics have argued that the benefits of including the vaccine in the national program are small in comparison to the benefits of other measures for which similar government resources could be used. Government’s concerns about the cost-utility of HPV vaccine have included the following: • There is a relatively low incidence of cervical cancer in Israel—(5.6/100,000 which corresponds to 222 new cases per year)—in comparison to the global average and North American incidence of cervical cancer (15.2/100,000 and 5.7/100,000 respectively [1,2]). • Currently, vaccines provide immunity against only two or four HPV types. • There is a high religiously normative circumcision rate (80%) in Israel, which is believed to contribute to the lower incidence of HPV infection in the country [14]. For maximum benefit, HPV vaccination is recommended for a vaccine target age range aimed at the time prior to the onset of sexual activity [15] and preferably in the national school-based vaccine program. In Israel within the national school-based vaccination program, compliance for other vaccines is in excess of 90% [15–17]. However, introducing HPV vaccine into Israel’s national school-based vaccine program might create difficulties due to the following: • Socially conservative parents are neither interested in vaccinating their children nor discussing the HPV vaccine with them because of their concern that, as a result of vaccination, their adolescent children would engage in promiscuous sexual behavior [18]. • Religious Jewish parents (comprising 25% of Israel’s population) may resist vaccination of their daughters for similar reasons. It has been shown that the more religious the mother, the lower the chance that she will vaccinate her daughter [18]. • The Israeli Arab community, almost 20% of the population [19], forbids sex before marriage, and would likely share concerns similar to those of socially conservative or religious Jewish parents about HPV vaccine promoting unrestricted sexual behavior in their children. • Supporting the likelihood of social or religious conservatism and resistance to HPV vaccination, a study [18] that examined the attitude of Israeli mothers towards HPV vaccination of their daughters found, as elsewhere [20], a correlation between mothers’ concern about promiscuity on the part of their daughters following vaccination and their lack of intention to vaccinate their daughters against HPV. Other potential barriers to HPV vaccination in Israel, in common with some other Western countries, include the following: • The influence of general practitioners, who can exert considerable influence on HPV vaccinating decisions made by families under their care, but who do not uniformly or proactively recommend the vaccine [21]. • In Israel, the influence of the anti-vaccine movement, which bases its opposition to vaccination on fear of side effects and on antivaccine ideology, is small, as indicated by the very high rate of vaccination uptake and population coverage with other vaccines administered in Israel [17]. However, the anti-vaccine movement may exert some effect on HPV vaccine acceptance in Israel and may see social conservatives’ ambivalence about HPV vaccine as a promising asset in its opposition to vaccination.
W.A. Fisher et al. / Vaccine 31S (2013) I53–I57
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Table 2 Perceptions of advantages and disadvantages of undergoing HPV vaccination in unvaccinated Israeli young women in the coming yeara (N = 55). Advantages
N
%b
Disadvantages
N
%b
Prevent cervical cancer Prevent health threat Prevent HPV infection Avoid infecting others Gynecologist recommended
33 33 15 3 2
60.0 60.0 27.3 5.5 3.6
Fear vaccine side effects Cost of the vaccine Vaccine too new Doubt all vaccines, therapies Too time consuming Dislike shots Not needed
32 16 16 11 9 7 5
58.2 29.1 29.1 20.0 16.4 12.7 9.1
a Based on Laniado H, 2012. Understanding the relationship between personal attitudes, subjective norms, perceive control, and intentions to be vaccinated against HPV [in Hebrew]. Unpublished master’s thesis, Dep. of Psychology, Tel Aviv University, Tel Aviv, Israel. b The column does not sum to 100% because respondents could choose multiple responses.
3. Public health education Lack of knowledge about HPV and its serious sequelae and lack of knowledge about the safety and efficacy of HPV vaccine may be additional reasons for limited uptake of the vaccine among young adult women in Israel [20,21]. An Israeli market research study initiated by Merck Sharp & Dohme (MSD) Israel of 300 mothers of daughters 12–20 years of age, conducted prior to vaccine launch (May 2006), showed very low awareness of cervical cancer and HPV related disease [22]. Increasing disease awareness appeared to be initial challenge for HPV vaccination for both health care providers and pharmaceutical manufacturers. Accordingly, the first HPV public health campaign in Israel emphasized disease awareness. The campaign, organized by a pharmaceutical company, was named “Tell someone”, and aimed to reach mothers of daughters aged 9–26, and young females aged 19–26 directly. The campaign included advertisements appearing in radio, newspapers and magazines. Consumers were encouraged to tell someone they know that cervical cancer is caused by HPV and to deepen their knowledge through either a website [23] and/or a toll free telephone number. In order to attach appropriate emotions of concern and vigilance to the subject of cervical cancer, patients’ testimonials were employed. The next campaign, named “One Less”, focused on prevention of HPV through vaccination. The campaign was carried out via TV, radio, internet, and by distributing postcards at health maintenance organization clinics. After the two campaigns, a post-campaign market research telephone survey was conducted, targeting two audience groups: 300 mothers of girls aged 9–26 and 300 adolescent and young adult women aged 16–26. Interestingly, although the survey showed that the level of awareness of the vaccine was high, the actual vaccination rate was low and stood at only about ten percent. The main reported barrier was the vaccine’s high cost [22]. 4. An initial Israeli HPV vaccine acceptability study: Attitudes, social support, and intentions to be vaccinated in a sample of Israeli undergraduate women HPV vaccine acceptability has been studied in a variety of patient and provider populations and from the perspective of a number of health behavior models [21,24–26], but research on correlates of HPV vaccine acceptability among vaccine age Israeli women is lacking. The present analysis is based upon the Theory of Reasoned Action and the Theory of Planned Behavior [27–33], two wellarticulated and well-researched models that have been successfully applied to understanding and predicting health behavior uptake. According to the Theory of Reasoned Action, an individual’s behavior—in this case, HPV vaccine uptake—is a function of the individual’s behavioral intentions. Behavioral intentions, in turn, are a function of attitudes toward personally engaging in the behavior in question and/or the individual’s perceptions of social
support from important others for the act in question. According to the Theory of Planned Behavior, behavior is again a function of behavioral intentions. However, behavioral intentions are seen as jointly influenced by attitudes towards the act, perceived social support, and perceived ability to actually undertake the act in question (termed perceived behavioral control). The contribution of perceived behavioral control may be particularly relevant when cost and other challenges and complexities are involved in engaging in a particular behavior, such as may be the case with respect to HPV vaccine uptake. A preliminary, recently conducted study in a small convenience sample of Israeli female undergraduates was conducted to empirically test the assumption that HPV vaccination intentions are function of attitudes towards personally undergoing vaccination, and/or perceptions of social support for doing so, and/or perceived ability to receive the vaccination (Laniado H, 2012. Understanding the relationship between personal attitudes, subjective norms, perceive control, and intentions to be vaccinated against HPV [in Hebrew]. Unpublished master’s thesis, Dep. of Psychology, Tel Aviv University, Tel Aviv, Israel). A sample of female Israeli undergraduates (N = 86), in the target age range for HPV vaccination (ages ranged from 21 to 24 years), participated in this research. For the current analysis, 55 out of 86 women—those who had not been vaccinated against HPV—comprised the sample of interest. These unvaccinated women completed measures of their intention to be vaccinated during the coming year, their attitudes towards being vaccinated during this time, their perceptions of social support for being vaccinated, and their perceptions of personal control or ability to be vaccinated. These women were also asked open-ended questions about their perceptions of the advantages or disadvantages of vaccination and about which significant others might support or oppose their vaccination. Questionnaire items were constructed and administered in accord with standard procedures to assessing and testing the components of the Theory of Reasoned Action and the Theory of Planned Behavior [21,26,29]. As can be seen in Table 2, Israeli undergraduate women who had not been vaccinated most commonly perceived the prevention of cervical cancer, prevention of health threat in general, and prevention HPV infection per se, to be advantages of undergoing HPV vaccination personally in the coming year. Commonly reported disadvantages of personally getting vaccinated in the coming year included fear of vaccine side effects, cost of the vaccine, and newness of the vaccine; and doubts about all vaccines and therapies. Time required to undergo multiple vaccinations and dislike of injections were represented as disadvantages as well. When comparing Israeli young women who intended to be vaccinated in the coming year (20 out of 55) with those who did not intend to be vaccinated during this interval (35 out of 55), women who intended to be vaccinated were significantly more likely to cite avoidance of future health threat as a primary advantage of being vaccinated (p-value < 0.05). Women who intended to be vaccinated were also substantially less likely to report that feared side effects
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W.A. Fisher et al. / Vaccine 31S (2013) I53–I57
Table 3 Perceptions of social support for undergoing HPV vaccination in unvaccinated Israeli young women in the coming yeara (N = 55). Support My Vaccination
N
%b
Oppose My Vaccination
N
%b
Friends Mother Doctor Partner Media
39 29 15 14 2
70.9 52.7 27.3 25.5 3.6
No one Mother Friends Doctor
20 12 4 4
36.4 21.8 7.3 7.3
a Based on Laniado H, 2012. Understanding the relationship between personal attitudes, subjective norms, perceive control, and intentions to be vaccinated against HPV [in Hebrew]. Unpublished master’s thesis, Dep. of Psychology, Tel Aviv University, Tel Aviv, Israel. b The column does not sum to 100% because respondents could choose multiple responses.
were a disadvantage of getting vaccinated (p-value < 0.05) (data not shown). Israeli young women who had not been vaccinated commonly perceived social support for getting HPV vaccination in the coming year from friends, mothers, doctors, and partners (Table 3). The modal source of social opposition to getting HPV vaccine was “no one,” although mother, friend, and doctor were reported opposing vaccination in some cases. When comparing young Israeli women who intended to be vaccinated in the coming year (20 out of 55) with those who did not (35 out of 55), women who intended to be vaccinated were more likely to perceive social support from their physicians (p-value < 0.05) (data not shown). A multiple regression analysis of personal attitudes, perceptions of social support, and perceived control on intentions to be vaccinated was conducted. This analysis revealed that Israeli young women’s attitudes to personally getting HPV vaccination (p-value < 0.001), but not their perceptions of social support for doing so (p-value = 0.17) or their perceived control or ability to do so (p-value = 0.16), contributed to their intentions to be personally vaccinated during the coming year. The multiple correlation of attitudes, norms, and perceived control with intentions to be vaccinated was 0.7, with personal attitudes the only factor contributing significantly to this relationship, and accounting for some 49% of the total variance in women’s intentions to be vaccinated. The current findings are preliminary and generalization beyond the sample of university undergraduate women under study is likely to be limited. At the same time, however, findings do illustrate the strength of attitudes as a correlate of vaccine intentions, and this general conceptual and methodological approach may readily be applied to various Israeli vaccine age target groups to identify attitudinal, normative, and perceived control or ability correlates of intentions to be vaccinated. 5. Conclusions Societal and individual barriers to HPV vaccination in Israel include Israel’s comparatively low incidence of cervical cancer, the vaccine’s high cost and its perceived association with unacceptable sexual relations. Governmental considerations involve, in addition to the low incidence of cervical cancer in Israel, cost-utility issues, such as the religiously-based high (80%) circumcision rate, which is thought to contribute to the low incidence of HPV infection and the limited immunity of the vaccine against only few HPV types. The literature and our findings also suggest that parental, patient, and physician motivation to seek, offer, or recommend HPV vaccination is implicated in acceptance of this vaccine. Initial research conducted with a small sample of Israeli undergraduate women confirms that motivation to be vaccinated—that is, personal attitudes towards undergoing vaccination in the coming year, which appear to be related to perceived health advantages and
absence of side effects—is strongly correlated with intentions to be vaccinated. At the same time, while perceptions of social support or opposition to vaccination were reported, and perceived ability to be vaccinated was explored as well, they added no unique variance to the prediction of young Israeli women’s intentions to be vaccinated. Disclosed potential conflicts of interest WAF: Has received consultant, travel, and research funding from Merck Canada. HL: Has disclosed no potential conflicts of interest. HS: Participated in a media intervention program sponsored by MSD Israel. MH: Has disclosed no potential conflicts of interest. JB: Has been a researcher for Merck & Co. (MSD) and GlaxoSmithKline (GSK) Israel. References [1] Ferlay J, Shin HR, Bray F, Forman D, Mathers C, Parkin DM. GLOBOCAN 2008 v2.0, Cancer Incidence and Mortality Worldwide: IARC CancerBase No. 10 [Internet]. Lyon, France: International Agency for Research on Cancer; 2010. Available at: http://globocan.iarc.fr (last accessed June 2013). [2] Shavit O, Roura E, Barchana M, Diaz M, Bornstein J. Burden of human papillomavirus infection and related diseases in Israel. Vaccine 2013;31S: I32–41. [3] Forman D, de Martel C, Lacey CJ, Soerjomataram I, Lortet-Tieulent J, Bruni L, et al. Global burden of human papillomavirus and related diseases. Vaccine 2012;20(30 Suppl 5):F12–23. [4] Shavit O, Raz R, Stein S, Chodick G, Schejter E, Cohen R, Shalev V. Evaluating the epidemiology and morbidity burden associated with human papillomavirus in Israel: accounting for CIN1 and genital warts in addition to CIN 2/3 and cervical cancer. Ppl Health Econ Health Policy 2012;10:87–97. [5] Huang CM. Human papillomavirus and vaccination. Mayo Clinic Proc 2008;83:701–7. [6] Kahn JA, Rosenthal SL, Jin Y, Huang B, Namakydoust A, Zimet GD. Rates of human papillomavirus vaccination, attitudes about vaccination, and human papillomavirus prevalence in young women. Obstet Gynecol 2008;111: 1103–10. [7] Conroy K, Rosenthal SL, Zimet GD, Jin Y, Bernstein DI, Glynn S, et al. Human papillomavirus vaccine uptake, predictors of vaccination, and self-reported barriers to vaccination. J Women’s Health 2009;18:1679–86. [8] Centers for Disease Control and Prevention. National and state vaccination coverage among adolescents aged 13 through 17 years - United States, 2010. MMWR 2011;60:1117–23. [9] Jain N, Euler GL, Shefer A, Lu P, Yankey D, Markowitz L. Human papillomavirus (HPV) awareness and vaccination initiation among women in the United States. National Immunization Survey-Adult 2007 Prev Med 2009;48:426–31. [10] Srugo I, Ashkenazi S, Bornstein J, Miron D, Stein M. Guidelines for HPV vaccination of the task force on pediatric HPV vaccination. Israeli Journal of Pediatrics 2009;67:2–4. [11] Bornstein J, Shavit O. Human papillomavirus-associated diseases in Israel – the controversy continues. Vaccine 2013;31S:v–viii. [12] Ginsberg GM, Fisher M, Ben-Shahar I, Bornstein J. Cost-utility analysis of vaccination against HPV in Israel. Vaccine 2007;25:6677–91. [13] The 312 seating of the 18th Knesset. Available at: www.knesset.gov.il/ plenum/data/05570811.doc (last accessed June 2013). [14] Albero G, Villa LL, Lazcano-Ponce E, Fulp W, Papenfuss MR, Nyitray AG, et al. Male circumcision and prevalence of genital human papillomavirus infection in men: a multinational study. BMC Infect Dis 2013;13:18. [15] Gamett P. Role of herd immunity in determining the effect of vaccines against sexually transmitted disease. J Infect Dis 2005;191(1):S97–106. [16] National Council for Children’s Welfare, Center for Research and Development. Children in Israel 2010, Statistical Yearbook. December 2010, Jerusalem [in Hebrew]. [17] Stein-Zamir C, Zentner G, Tallen-Gozani E, Grotto I. The Israel National Immunization Registry. Isr Med Assoc J 2010;12:296–300. [18] Ben Natan M, Aharon O, Palickshvili S, Gurman V. Attitude of Israeli mothers with vaccination of their daughters against human papilloma virus. J Pediatr Nurs 2011;26(1):70–7. [19] Israeli population by groups. Israel central bureau of statistics. Available at: http://www.cbs.gov.il/yarhon/b1 h.htm (last accessed June 2013). [20] Zimet GD, Weiss TW, Rosenthal SL, Good MB, Vichnin MD. Reasons for nonvaccination against HPV and future vaccination intentions among 19-26 yearold women. BMC Women’s Health 2010;10:27. [21] Rosenthal SL, Weiss TW, Zimet GD, Ma L, Good MB, Vichnin MD. Predictors of HPV vaccine uptake among women ages 19-26: importance of a physician’s recommendation. Vaccine 2011;29:890–5.
W.A. Fisher et al. / Vaccine 31S (2013) I53–I57 [22] Merck Sharp & Dohme Israel. Available at: http://www.msd.co.il/ (last accessed June 2013). [23] HPV website from Merck Sharp & Dohme Israel. Available at: www.hpv.co.il (last accessed June 2013). [24] Donovan B, Franklin N, Guy R, Grulich AE, Regan DG, Ali H, et al. Quadrivalent human papillomavirus vaccination and trends in genital warts in Australia: analysis of national sentinel surveillance data. Lancet Infect Dis 2011;11(1):39–44. [25] Black LL, Zimet GD, Short MB, Sturm L, Rosenthal SL. Literature review of human papillomavirus vaccine acceptability among women over 26 years. Vaccine 2009;27:1668–73. [26] Gilbert P, Brewer NT, Reiter PL, Ng TW, Smith JS. HPV vaccine acceptability in heterosexual, gay, and bisexual men. Am J Mens Health 2011;5:297–305. [27] Fishbein M, Ajzen I. Belief, attitude, intention and behavior: An introduction to theory and research. Reading, MA: Addison-Wesl; 1975.
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[28] Ajzen I, Fishbein M. Understanding attitudes and predicting social behavior. Prentice Hall: Englewood Cliffs, NJ; 1980. [29] Sheppard BH, Hartwick J, Warshaw PR. The theory of reasoned action: A metaanalysis of past research with recommendations for modifications for future research. J Consum Res 1988;15:325–43. [30] Albarracin D, Fishbein M, Johnson BT, Muellerleile PA. Theory of Reasoned Action and Theory of Planned Behavior as models of condom use: A metaanalysis. Psychol Bull 2001;147(1):142–61. [31] Ajzen I. Theory of planned behavior. Organ Behav Hum Dec 1991;50: 179–211. [32] Ajzen I, Madden TJ. Prediction of goal-directed behavior: Attitudes, intentions, and perceived behavioral control. J Exp Soc Psych 1986;22:453–74. [33] Armitage CJ, Conner M. Efficacy of the theory of planned behaviour: A metaanalytic review. Br J Soc Psych 2001;40:471–99.
Contents lists available at ScienceDirect
Vaccine journal homepage: www.elsevier.com/locate/vaccine
Review
Barriers to Human Papillomavirus Vaccine Acceptability in Israel William A. Fisher a , Hila Laniado b , Hila Shoval c , Marwan Hakim d,e , Jacob Bornstein e,f,∗ a
Department of Psychology and Department of Obstetrics and Gynecology, University of Western Ontario, London Ontario, Canada Department of Psychology, Tel Aviv University, Tel Aviv, Israel c Medical Scientific Liaison, M.S.D., Israel d The Nazareth Hospital, Nazareth, Israel e Bar-Ilan University Galilee Faculty of Medicine, Nahariya, Israel f Department of Obstetrics and Gynecology, Western Galilee Hospital, Nahariya, Israel b
a r t i c l e
i n f o
Article history: Received 1 February 2012 Received in revised form 6 June 2012 Accepted 18 June 2013 Keywords: Israel HPV vaccine acceptability HPV Cervical cancer Circumcision Attitudes Social support
a b s t r a c t Barriers to human papillomavirus (HPV) vaccine acceptability in Israel include Israel’s relatively low incidence of cervical cancer; the religiously-based 80% circumcision rate in Israel, which is regarded as contributing to the lower incidence of HPV infection in the country; the fact that HPV vaccine provides immunity against only few virus types; the vaccine’s high cost; and the perception that HPV transmission is associated with unacceptable sexual relations. A recent survey has demonstrated that, following media two campaigns, Israeli’s level of awareness of the vaccine increased but the actual vaccination rate remained low, at approximately 10%. Survey findings also indicated that an enduring barrier to HPV vaccination is the vaccine’s high cost. Recent research on a convenience sample of Israeli undergraduate women 21 to 24 years of age showed that intentions to receive HPV vaccination in the coming year were a function of women’s attitudes towards getting vaccinated and their perceptions of social support for doing so. Undergraduate women who intended to be vaccinated perceived the prevention of cervical cancer, avoidance of personal health threat, and avoidance of HPV infection per se to be the advantages of undergoing HPV vaccination. Disadvantages of getting vaccinated included fear of vaccine side effects, cost of the vaccine, and newness of the vaccine, doubts about vaccines, time required to undergo multiple vaccinations, and dislike of injections. Friends’, mothers’ and physicians’ recommendations influenced women’s intentions to be vaccinated in the coming year as well. This article forms part of a regional report entitled “Comprehensive Control of HPV Infections and Related Diseases in Israel” Vaccine Volume 31, Supplement 8, 2013. Updates of the progress in the field are presented in a separate monograph entitled “Comprehensive Control of HPV Infections and Related Diseases” Vaccine Volume 30, Supplement 5, 2012. © 2013 Elsevier Ltd. All rights reserved.
1. Introduction There are some 2.47 million women aged 15 years and older in Israel and estimates for 2008 indicated that approximately 222 women were diagnosed with cervical cancer and about 98 women died from the disease each year [1,2]. By 2025, Israel is projected to experience 302 new cervical cancer cases and 141 cervical cancer deaths per year [1,2]. In addition to cervical cancer, human papillomavirus (HPV) contributes to a portion of Israel’s vulvar, vaginal, and anal cancer cases (Table 1) [1–3]. HPV types 6 and 11 are also the dominant cause of HPV related genital warts in Israel [3]. A recent retrospective study revealed that the annual occurrence of genital warts in Israel is about 17,430 cases [4].
∗ Corresponding author. Tel.: +972 4 9107720; fax: +972 4 9107472. E-mail address: [email protected] (J. Bornstein). 0264-410X/$ – see front matter © 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.vaccine.2013.06.107
The two HPV vaccines currently approved for use in Israel include a bivalent vaccine to protect against HPV 16 and 18 infection (Cervarix® , GlaxoSmithKline Biologicals, Rixensart, Belgium) and a quadrivalent vaccine against HPV 6, 11, 16, and18 infection (Gardasil® , Merck & Co., Whitehouse Station, NJ, USA). The vaccines appear to provide some cross-protection against other HPV types, especially against HPV 31 (both vaccines), 33 and 45 (bivalent vaccine), which are phylogenetically related to HPV 16 and 18. The two vaccines are accessible in the private market and are partially covered by supplementary health insurance policies. To promote vaccine uptake, the Advisory Committee on Immunization Practices (ACIP) in the United States recommended universal vaccination of all 11–12 year-old girls as part of routine preventive care visits, and comprehensive “catch-up” vaccination of adolescent and young adult women between the ages of 13 and 26 years [5]. Despite ACIP recommendation, vaccination coverage rates in the United States remain low: in 2010, 47.7% of 13–17 yearold girls had received one or more doses of HPV vaccine. Of those
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W.A. Fisher et al. / Vaccine 31S (2013) I53–I57
Table 1 Annual incidence of HPV-related anogenital cancers and HPV attributable cases in Israel. Cancer type Cervical Vulvar Vaginal Anal Total
Number of new cases per year 222a 48b 12b 20b 302
% HPV-attributable 100c 43c 70c 88c 89d
Number of annual cases attributed to HPV 222 21 8 18 269
a
Estimated incidence cases for 2008. GLOBOCAN 2008 [1]. Estimated incidence cases for the period 1998-2002 [2]. c HPV-attributable fraction from Forman D et al. [3]. d Calculated as the total number of annual cases attributed to HPV divided by the total number of anogenital cases per year. b
who had received one dose and were eligible to complete the series, 73.2% received all three doses [6–9]. In Israel, private vaccination coverage rates remain low, at around 10% of eligible women. The Israeli Pediatrics Infectious Disease Society and the Israel Association of Obstetrics and Gynecology have published position papers supportive of HPV vaccination [10]. The Israeli national vaccination committee recommended introduction of HPV vaccination as part of the national immunization program and it will be introduced free of charge to the school-based vaccine program in September 2013. The objective of the current paper is to review barriers to HPV vaccination and report on a preliminary study of factors that influence HPV vaccine acceptability in Israel. 2. Barriers to HPV vaccination in Israel A number of barriers to HPV vaccination appear to work against vaccine acceptance in Israel. Without widespread acceptance, vaccination programs cannot take place, herd immunity to HPV will not occur, and HPV infection and sequelae of infection will persist. The following factors are society/individual issues that appear to work against HPV vaccine acceptance in Israel: • There is a relatively low incidence of cervical cancer in Israel (Bornstein J and Shavit O, Vaccine, 2013 [11] and Shavit O et al., Vaccine, 2013 [2]). • Current HPV vaccines are perceived to induce immunity to only a limited number of HPV types. • HPV vaccines are costly in Israel [12]. • The belief that HPV transmission and by extension HPV vaccination are closely associated with unacceptable sexual relations. The Israeli Ministry of Health approved HPV vaccination in 2007 and it will be introduced to the school-based immunization program for 13 year-old girls in September 2013. Until then, the burden of cost was left on the patients, who faced the challenge of covering the high cost of vaccination. The cost of HPV vaccine coverage in Israel currently is equivalent to $800 in the private market, while the average monthly wage is $2,000 [11]; thus, it is quite difficult to finance personal or programmatic vaccination in Israel, especially for the financially disadvantaged, who would have to pay up to $400 for the vaccine even with supplementary health insurance coverage. As HPV vaccination becomes part of Israel’s national school-based immunization program, a decrease in the burden of HPV-related disease is expected within the vaccinated cohort and, in time and via herd immunity, in the wider Israeli population. In the past, before the cost of the vaccine went down, the cost of supporting a national school-based vaccine program had been a main factor in the Israel Ministry of Health’s decision to decline funding of a national HPV vaccination program [13]. At the present
time, a number of additional factors appear to have contributed to resistance to the addition of HPV vaccine in Israel’s national immunization program. Critics have argued that the benefits of including the vaccine in the national program are small in comparison to the benefits of other measures for which similar government resources could be used. Government’s concerns about the cost-utility of HPV vaccine have included the following: • There is a relatively low incidence of cervical cancer in Israel—(5.6/100,000 which corresponds to 222 new cases per year)—in comparison to the global average and North American incidence of cervical cancer (15.2/100,000 and 5.7/100,000 respectively [1,2]). • Currently, vaccines provide immunity against only two or four HPV types. • There is a high religiously normative circumcision rate (80%) in Israel, which is believed to contribute to the lower incidence of HPV infection in the country [14]. For maximum benefit, HPV vaccination is recommended for a vaccine target age range aimed at the time prior to the onset of sexual activity [15] and preferably in the national school-based vaccine program. In Israel within the national school-based vaccination program, compliance for other vaccines is in excess of 90% [15–17]. However, introducing HPV vaccine into Israel’s national school-based vaccine program might create difficulties due to the following: • Socially conservative parents are neither interested in vaccinating their children nor discussing the HPV vaccine with them because of their concern that, as a result of vaccination, their adolescent children would engage in promiscuous sexual behavior [18]. • Religious Jewish parents (comprising 25% of Israel’s population) may resist vaccination of their daughters for similar reasons. It has been shown that the more religious the mother, the lower the chance that she will vaccinate her daughter [18]. • The Israeli Arab community, almost 20% of the population [19], forbids sex before marriage, and would likely share concerns similar to those of socially conservative or religious Jewish parents about HPV vaccine promoting unrestricted sexual behavior in their children. • Supporting the likelihood of social or religious conservatism and resistance to HPV vaccination, a study [18] that examined the attitude of Israeli mothers towards HPV vaccination of their daughters found, as elsewhere [20], a correlation between mothers’ concern about promiscuity on the part of their daughters following vaccination and their lack of intention to vaccinate their daughters against HPV. Other potential barriers to HPV vaccination in Israel, in common with some other Western countries, include the following: • The influence of general practitioners, who can exert considerable influence on HPV vaccinating decisions made by families under their care, but who do not uniformly or proactively recommend the vaccine [21]. • In Israel, the influence of the anti-vaccine movement, which bases its opposition to vaccination on fear of side effects and on antivaccine ideology, is small, as indicated by the very high rate of vaccination uptake and population coverage with other vaccines administered in Israel [17]. However, the anti-vaccine movement may exert some effect on HPV vaccine acceptance in Israel and may see social conservatives’ ambivalence about HPV vaccine as a promising asset in its opposition to vaccination.
W.A. Fisher et al. / Vaccine 31S (2013) I53–I57
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Table 2 Perceptions of advantages and disadvantages of undergoing HPV vaccination in unvaccinated Israeli young women in the coming yeara (N = 55). Advantages
N
%b
Disadvantages
N
%b
Prevent cervical cancer Prevent health threat Prevent HPV infection Avoid infecting others Gynecologist recommended
33 33 15 3 2
60.0 60.0 27.3 5.5 3.6
Fear vaccine side effects Cost of the vaccine Vaccine too new Doubt all vaccines, therapies Too time consuming Dislike shots Not needed
32 16 16 11 9 7 5
58.2 29.1 29.1 20.0 16.4 12.7 9.1
a Based on Laniado H, 2012. Understanding the relationship between personal attitudes, subjective norms, perceive control, and intentions to be vaccinated against HPV [in Hebrew]. Unpublished master’s thesis, Dep. of Psychology, Tel Aviv University, Tel Aviv, Israel. b The column does not sum to 100% because respondents could choose multiple responses.
3. Public health education Lack of knowledge about HPV and its serious sequelae and lack of knowledge about the safety and efficacy of HPV vaccine may be additional reasons for limited uptake of the vaccine among young adult women in Israel [20,21]. An Israeli market research study initiated by Merck Sharp & Dohme (MSD) Israel of 300 mothers of daughters 12–20 years of age, conducted prior to vaccine launch (May 2006), showed very low awareness of cervical cancer and HPV related disease [22]. Increasing disease awareness appeared to be initial challenge for HPV vaccination for both health care providers and pharmaceutical manufacturers. Accordingly, the first HPV public health campaign in Israel emphasized disease awareness. The campaign, organized by a pharmaceutical company, was named “Tell someone”, and aimed to reach mothers of daughters aged 9–26, and young females aged 19–26 directly. The campaign included advertisements appearing in radio, newspapers and magazines. Consumers were encouraged to tell someone they know that cervical cancer is caused by HPV and to deepen their knowledge through either a website [23] and/or a toll free telephone number. In order to attach appropriate emotions of concern and vigilance to the subject of cervical cancer, patients’ testimonials were employed. The next campaign, named “One Less”, focused on prevention of HPV through vaccination. The campaign was carried out via TV, radio, internet, and by distributing postcards at health maintenance organization clinics. After the two campaigns, a post-campaign market research telephone survey was conducted, targeting two audience groups: 300 mothers of girls aged 9–26 and 300 adolescent and young adult women aged 16–26. Interestingly, although the survey showed that the level of awareness of the vaccine was high, the actual vaccination rate was low and stood at only about ten percent. The main reported barrier was the vaccine’s high cost [22]. 4. An initial Israeli HPV vaccine acceptability study: Attitudes, social support, and intentions to be vaccinated in a sample of Israeli undergraduate women HPV vaccine acceptability has been studied in a variety of patient and provider populations and from the perspective of a number of health behavior models [21,24–26], but research on correlates of HPV vaccine acceptability among vaccine age Israeli women is lacking. The present analysis is based upon the Theory of Reasoned Action and the Theory of Planned Behavior [27–33], two wellarticulated and well-researched models that have been successfully applied to understanding and predicting health behavior uptake. According to the Theory of Reasoned Action, an individual’s behavior—in this case, HPV vaccine uptake—is a function of the individual’s behavioral intentions. Behavioral intentions, in turn, are a function of attitudes toward personally engaging in the behavior in question and/or the individual’s perceptions of social
support from important others for the act in question. According to the Theory of Planned Behavior, behavior is again a function of behavioral intentions. However, behavioral intentions are seen as jointly influenced by attitudes towards the act, perceived social support, and perceived ability to actually undertake the act in question (termed perceived behavioral control). The contribution of perceived behavioral control may be particularly relevant when cost and other challenges and complexities are involved in engaging in a particular behavior, such as may be the case with respect to HPV vaccine uptake. A preliminary, recently conducted study in a small convenience sample of Israeli female undergraduates was conducted to empirically test the assumption that HPV vaccination intentions are function of attitudes towards personally undergoing vaccination, and/or perceptions of social support for doing so, and/or perceived ability to receive the vaccination (Laniado H, 2012. Understanding the relationship between personal attitudes, subjective norms, perceive control, and intentions to be vaccinated against HPV [in Hebrew]. Unpublished master’s thesis, Dep. of Psychology, Tel Aviv University, Tel Aviv, Israel). A sample of female Israeli undergraduates (N = 86), in the target age range for HPV vaccination (ages ranged from 21 to 24 years), participated in this research. For the current analysis, 55 out of 86 women—those who had not been vaccinated against HPV—comprised the sample of interest. These unvaccinated women completed measures of their intention to be vaccinated during the coming year, their attitudes towards being vaccinated during this time, their perceptions of social support for being vaccinated, and their perceptions of personal control or ability to be vaccinated. These women were also asked open-ended questions about their perceptions of the advantages or disadvantages of vaccination and about which significant others might support or oppose their vaccination. Questionnaire items were constructed and administered in accord with standard procedures to assessing and testing the components of the Theory of Reasoned Action and the Theory of Planned Behavior [21,26,29]. As can be seen in Table 2, Israeli undergraduate women who had not been vaccinated most commonly perceived the prevention of cervical cancer, prevention of health threat in general, and prevention HPV infection per se, to be advantages of undergoing HPV vaccination personally in the coming year. Commonly reported disadvantages of personally getting vaccinated in the coming year included fear of vaccine side effects, cost of the vaccine, and newness of the vaccine; and doubts about all vaccines and therapies. Time required to undergo multiple vaccinations and dislike of injections were represented as disadvantages as well. When comparing Israeli young women who intended to be vaccinated in the coming year (20 out of 55) with those who did not intend to be vaccinated during this interval (35 out of 55), women who intended to be vaccinated were significantly more likely to cite avoidance of future health threat as a primary advantage of being vaccinated (p-value < 0.05). Women who intended to be vaccinated were also substantially less likely to report that feared side effects
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W.A. Fisher et al. / Vaccine 31S (2013) I53–I57
Table 3 Perceptions of social support for undergoing HPV vaccination in unvaccinated Israeli young women in the coming yeara (N = 55). Support My Vaccination
N
%b
Oppose My Vaccination
N
%b
Friends Mother Doctor Partner Media
39 29 15 14 2
70.9 52.7 27.3 25.5 3.6
No one Mother Friends Doctor
20 12 4 4
36.4 21.8 7.3 7.3
a Based on Laniado H, 2012. Understanding the relationship between personal attitudes, subjective norms, perceive control, and intentions to be vaccinated against HPV [in Hebrew]. Unpublished master’s thesis, Dep. of Psychology, Tel Aviv University, Tel Aviv, Israel. b The column does not sum to 100% because respondents could choose multiple responses.
were a disadvantage of getting vaccinated (p-value < 0.05) (data not shown). Israeli young women who had not been vaccinated commonly perceived social support for getting HPV vaccination in the coming year from friends, mothers, doctors, and partners (Table 3). The modal source of social opposition to getting HPV vaccine was “no one,” although mother, friend, and doctor were reported opposing vaccination in some cases. When comparing young Israeli women who intended to be vaccinated in the coming year (20 out of 55) with those who did not (35 out of 55), women who intended to be vaccinated were more likely to perceive social support from their physicians (p-value < 0.05) (data not shown). A multiple regression analysis of personal attitudes, perceptions of social support, and perceived control on intentions to be vaccinated was conducted. This analysis revealed that Israeli young women’s attitudes to personally getting HPV vaccination (p-value < 0.001), but not their perceptions of social support for doing so (p-value = 0.17) or their perceived control or ability to do so (p-value = 0.16), contributed to their intentions to be personally vaccinated during the coming year. The multiple correlation of attitudes, norms, and perceived control with intentions to be vaccinated was 0.7, with personal attitudes the only factor contributing significantly to this relationship, and accounting for some 49% of the total variance in women’s intentions to be vaccinated. The current findings are preliminary and generalization beyond the sample of university undergraduate women under study is likely to be limited. At the same time, however, findings do illustrate the strength of attitudes as a correlate of vaccine intentions, and this general conceptual and methodological approach may readily be applied to various Israeli vaccine age target groups to identify attitudinal, normative, and perceived control or ability correlates of intentions to be vaccinated. 5. Conclusions Societal and individual barriers to HPV vaccination in Israel include Israel’s comparatively low incidence of cervical cancer, the vaccine’s high cost and its perceived association with unacceptable sexual relations. Governmental considerations involve, in addition to the low incidence of cervical cancer in Israel, cost-utility issues, such as the religiously-based high (80%) circumcision rate, which is thought to contribute to the low incidence of HPV infection and the limited immunity of the vaccine against only few HPV types. The literature and our findings also suggest that parental, patient, and physician motivation to seek, offer, or recommend HPV vaccination is implicated in acceptance of this vaccine. Initial research conducted with a small sample of Israeli undergraduate women confirms that motivation to be vaccinated—that is, personal attitudes towards undergoing vaccination in the coming year, which appear to be related to perceived health advantages and
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