- Email: [email protected]
Attitudes towards HPV immunization of Italian mothers of adolescent girls and potential role of health professionals in the immunization program
Vaccine 27 (2009) 2625–2629
Contents lists available at ScienceDirect
Vaccine journal homepage: www.elsevier.com/locate/vaccine
Attitudes towards HPV immunization of Italian mothers of adolescent girls and potential role of health professionals in the immunization program Alberto E. Tozzi ∗ , Lucilla Ravà, D. Stat, Elisabetta Pandolfi, Maria G. Marino, Alberto G. Ugazio Bambino Gesù Hospital, Rome, Italy
a r t i c l e
i n f o
Article history: Received 5 November 2008 Received in revised form 19 January 2009 Accepted 18 February 2009 Available online 24 February 2009 Keywords: HPV vaccine Adolescents Mothers Immunization strategy
a b s t r a c t We assessed the knowledge of Italian mothers of adolescent girls about HPV and HPV vaccination, their willingness to immunize their daughters, and their perception of the role of different medical specialists in the HPV immunization strategy by a telephone interview. Fifty-four percent of the 807 interviewed mothers reported to have ever heard about HPV, and 84% of them were willing to immunize their daughters. Pediatricians most frequently provided information on HPV vaccine (31%), and were perceived as the preferred immunization providers (77%). Acceptance of HPV immunization was high and was not associated with knowledge of HPV. © 2009 Elsevier Ltd. All rights reserved.
1. Introduction The recent implementation of HPV immunization programs in several industrialized countries has resulted so far in a moderate success in terms of vaccination uptake [1,2]. However, since the public health impact of HPV immunization will be greatest if a high coverage of the target population is achieved [3], it is important to identify efficient strategies, suitable for local settings, to maintain and improve HPV immunization coverage. Information strategies are crucial for promoting immunizations. HPV vaccination, however, poses an unusual challenge because it targets female adolescents only and prevents a disease which may occur several decades after immunization, and because related information strategies necessarily touch sensitive issues such as sexual behaviours which parents may be concerned about [4]. Several studies of parental attitudes – mostly carried out in the US – suggest that most parents are in favour of immunizing their children [4–11], although they would need more information [9–11]. Physician recommendation has been considered a strong predictor of vaccine acceptance by parents of girls in the target population [4,12], and several studies have shown that pediatricians, family
∗ Corresponding author at: Bambino Gesù Hospital, Epidemiology Unit, Piazza S. Onofrio 4, 00165 Rome, Italy. Tel.: +39 06 68592401; fax: +39 06 68592853. E-mail address: [email protected] (A.E. Tozzi). 0264-410X/$ – see front matter © 2009 Elsevier Ltd. All rights reserved. doi:10.1016/j.vaccine.2009.02.050
physicians, and gynecologists support HPV immunization [13–16]. Although integration among different health professionals has been recommended in HPV immunization strategies [17,18], studies concerning the attitude towards HPV vaccination have not satisfactorily addressed the parents’ perception of the roles played by specific specialists. In Italy, a local family pediatrician of the National Health System is responsible for delivering primary care until the age of 14. Although most children remain assigned to family pediatricians until this age, families may decide to shift their children to a general practitioner for primary care from the age of 6 years. Other medical specialists of the National Health System, including gynecologists, are consulted in case of need, possibly after an indication by the primary care physician. Immunizations for the general population are delivered in public immunization practices by public health specialists, though 5% of parents opt for immunization in private practices [19]. A national HPV immunization program has recently begun in Italy. In spring 2007 the Ministry of Health started an information campaign that included advertisements on the media and internet web sites. Active offer of HPV immunization to adolescent girls born in 1997 actually started in early 2008. We carried out a cross-sectional study on a large sample of mothers of adolescent girls from all over the country in late 2007, after the information campaign, and before the beginning of the immunization program. Aims of the study were to assess parents’ knowledge about HPV and HPV vaccination and their willingness to have their
2626
A.E. Tozzi et al. / Vaccine 27 (2009) 2625–2629
daughters immunized, and to investigate the roles of the different medical specialists in the immunization strategy as perceived by parents. 2. Methods 2.1. Population and study design We identified as the target population of the study mothers living in any Italian Region with a daughter aged 10–12 years at the time of the interview. Additional eligibility criteria for participation in the study included ability to speak Italian, and availability of a telephone line. For the interview we used a convenience sample of mothers who already participated in other medical surveys and who previously declared their availability to participate in other knowledge, attitude, and practice studies. Mothers were progressively and randomly extracted from a database including 4809 names meeting eligibility criteria until the desired sample size was met, and received a telephone call by a trained operator for the administration of a telephone questionnaire. In case of no answer, a total of three attempts were made to have a successful contact after which the family was withdrawn. Questionnaires were administered from October to December 2007 after obtaining a verbal informed consent. 2.2. Survey questionnaire A 29-item semistructured telephonic questionnaire was used to assess attitudes and knowledge about HPV vaccines, sociodemographic characteristics, and perceived role of medical specialists in providing information and administering HPV vaccine. Some of the answers concerning whom the mothers would prefer their daughters to be vaccinated by, and whom they would prefer as information provider about HPV were open ended and were recoded in categories during the analysis. For these questions the interviewer did not suggest any clue. The interview took approximately 15 min to be completed. 2.3. Sample size and statistical analysis The primary outcomes measured in this study were parental knowledge of HPV and acceptability of HPV vaccines. We calculated that a sample size of 800 mothers would have been sufficient to detect a 50% proportion with knowledge of HPV or willing to accept HPV vaccination for their daughters with a precision of ±4%. Proportions and their 95% confidence intervals were compared through the chi-square test. A multivariate logistic regression analysis was used to determine significant independent predictors of parental knowledge about HPV and acceptability of HPV vaccine. We included in the multivariate analysis sociodemographic variables such as parents’ and child age, parents’ educational level and job, and geographical area of residence. Since it has been suggested that use of Pap-test in mothers may influence their attitude to vaccinate their daughters [6], we also included among independent variables mother’s Pap-test frequency. Finally, we included in the models a variable related to occurrence of child menarche as an indicator of sexual maturity, and the number of visits in the pediatrician’s office in the last 12 months. For the model on attitude towards HPV vaccine, mother’s knowledge of HPV was also included among independent variables. For the purpose of the multivariate analysis, in yes/no/don’t know items, the “no” and “don’t know” answers were grouped together. All data were analyzed using STATA9 (Stata Corp, College Station, TX) statistical software.
3. Results A total of 878 mothers were contacted, and 807 (91.9%) of them accepted to complete the interview. The general characteristics of mothers participating in the study are illustrated in Table 1. Less than one quarter of families included more than one child, more than 15% of the interviewed mothers were single, most parents were white collars, and 53–61% of them had a high school diploma. Our sample showed a slightly higher parent education level compared with the national general population [20]. Less than 10% of the mothers included in the sample never had a Paptest. This frequency was lower than that of the general population [21]. Results concerning knowledge of HPV and HPV immunization are illustrated in Table 2. The level of knowledge of HPV in interviewed mothers was modest: at least one-third stated they had never heard about HPV infection, and only one quarter of respondents declared to have sufficient information about HPV. More than 60% of mothers stated they knew about the national HPV immunization campaign. Interestingly this proportion was slightly higher than that of mothers who declared to have ever heard of human papillomavirus. Among the additional information that interviewed mothers would like to know more about, vaccine safety and efficacy were indicated by 48% and 44% of respondents respectively, while duration of protection was indicated by less than 10% of them. The proportion of mothers willing to accept HPV immunization for their daughters was close to 85%, and cost did not represent a barrier to vaccination since nearly the same proportion of them reported to be ready to pay for having their daughters vaccinated. Mothers who judged positively the immunization program reported prevention of cancer (67.0%) and prevention of a frequent infection (25.1%) as reasons to support HPV vaccination,
Table 1 Characteristics of the 807 interviewed mothers. Mean (S.D.; range) Age of daughters 10 years 11 years 12 years Post-menarchal girls Family with ≥2 children Single parent Mothers’ age Mothers’ educational level (high school diploma) Mothers’ profession Professional White collar Blue collar Housewife Father’s age Fathers’ educational level (high school diploma) Fathers’ profession Professional White collar and army Blue collar Unemployed
N (%) 207 (25.6) 447 (55.4) 153 (19.0) 482 (59.7) 184 (22.8) 133 (16.5)
39.4 (2.4; 31–47) 431 (53.4)
39 (4.8) 433 (53.7) 223 (27.6) 112 (13.9) 43.1 (3.7; 36–54) 494 (61.2)
48 (5.9) 496 (61.5) 212 (26.3) 51 (6.3)
Residency geographic area North Middle South and islands
319 (39.5) 163 (20.2) 325 (40.3)
Mother’s Pap-test frequency Regularly At least once in the life Never
416 (51.5) 326 (40.4) 65 (8.1)
A.E. Tozzi et al. / Vaccine 27 (2009) 2625–2629 Table 2 HPV knowledge and attitude of interviewed mothers.
Only 8.6% of them felt that the vaccine would encourage sexual promiscuity. Table 3 shows the information source on HPV and HPV vaccine reported by interviewed mothers. Newspapers and magazines were the most frequent information source on HPV and HPV immunization. Gynecologists and general practitioners were an information source for HPV in more than 45% of mothers, whereas pediatricians and gynecologists accounted for nearly 41% of the information sources for HPV vaccination. A proportion of 2.5% of the mothers reported they knew HPV because they had experienced an abnormal Pap-test. Radio, television, and the internet were rarely reported as an information source. Table 4 shows the preferred medical specialist by whom mothers would like to be informed on HPV and HPV immunization. Gynecologists were perceived as the preferred source of additional information on both HPV and HPV immunization. The role of general practitioners was also substantial. Although immunizations are not usually provided by pediatricians in Italy, 620 interviewed mothers (76.8%) reported they would prefer them as HPV immunization providers for their daughters, 124 (15.4%) would prefer general practitioners, 58 (7.2%) public health immunization providers, and 5 (0.6%) gynecologists. All daughters of interviewed mothers were visited at least once in a pediatrician office in the 12 months preceding the interview. A total of 267 mothers (33%) declared also that their daughters were visited by other specialists in the previous 12 months. They were most frequently ophthalmologists (27.3%), allergologists (18.0%), and dentists (17.6%). None of the children were seen by a gynaecologist. The multivariate analyses showed that the variables included in the models poorly explained knowledge of HPV infection or HPV immunization acceptance. Knowledge of HPV infection was associated with mother’s age only (OR: 1.1; 95% CI: 1.0–1.2), and HPV immunization acceptance showed no associations with any of the variables included in the model.
N (%) Have you ever heard about human papillomavirus? Yes 437 (54.1) No 270 (33.5) Don’t know 100 (12.4) Would you say you have sufficient information on HPV? Yes 106 (24.3) No 217 (49.7) Don’t know 114 (26.1) Which additional information would you like most to have on HPV vaccine (open ended)? Vaccine safety 387 (48.0) Vaccine efficacy 352 (43.6) Duration of protection 62 (7.7) Other 6 (0.7) Did you know that the Ministry of Health is going to offer an HPV vaccine to 12 years old girls for free? Yes 507 (62.8) No 196 (24.3) Don’t know 104 (12.9) Will you accept the active offer of the HPV vaccine for your daughter? Yes 675 (83.6) No 35 (4.3) Don’t know 97 (12.0) If your daughter was out of the age range for free HPV immunization, would you pay to vaccinate her? Yes 673 (83.4) No 35 (4.3) Don’t know 99 (12.3)
while prevention of genital warts was reported by only 6.4% of supportive mothers. Mothers against the immunization program were concerned about administering too many vaccines (54.3%), and felt that Pap-test was sufficient to prevent cancer (31.4%). Table 3 Information source on HPV and HPV vaccine. Source
4. Discussion N (%)
The results of this study show a good attitude towards HPV vaccination but a definitely poor knowledge level about HPV in the interviewed mothers. The level of knowledge on HPV measured in our study was however higher than that recently reported in a study performed in Italian women [22]. Contrarily to the results of other studies [4,23], less than 10% of the interviewed mothers who were not in favour of HPV immunization feared to encourage sexual promiscuity of their daughters through vaccination, while most of them were worried about the high number of vaccines received. Interestingly, in our study vaccine cost was not perceived as a barrier to immunization, although mothers were informed that cost per dose was approximately 100–120 euros. Only mothers’ age was associated with a better knowledge of HPV, and none of the variables considered in our analysis predicted a positive attitude towards HPV vaccine. Other studies reported contradictory evidence on the efficacy of information strategies on the improvement of the immunization uptake [24,25]. Since knowledge on HPV was not associated with vaccination acceptance,
Who or what was your information source on HPV (open ended)?a Newspapers/magazines 146 (33.4) Gynecologist 116 (26.4) General practitioner 81 (18.5) Friends/relatives 43 (9.8) Radio/TV 32 (7.3) Abnormal Pap-test 11 (2.5) Who or what was your information source on the HPV vaccination program (open ended)?b Newspapers/magazines 193 (38.1) Pediatrician 157 (31.0) Gynecologist 51 (10.1) General practitioner 46 (9.1) Radio/TV 30 (5.9) Friends/relatives 21 (4.1) Internet 9 (1.8) a b
2627
429/437 responses of mothers who had heard about HPV. 507/507 responses of mothers who knew about the vaccination program.
Table 4 Preferred medical specialists for providing information on HPV and HPV immunization.
To which medical specialist would you ask more information on HPV (open ended)? To which medical specialist would you ask more information about HPV immunization (open ended)?
Gynecologist, N (%)
Pediatrician, N (%)
General practitioner, N (%)
Public health immunization provider, N (%)
324 (40.1)
201 (24.9)
242 (30.0)
40 (5.0)
538 (66.7)
5 (0.6)
210 (26.0)
54 (6.7)
2628
A.E. Tozzi et al. / Vaccine 27 (2009) 2625–2629
our findings suggest that improving parents’ knowledge may not increase vaccine acceptability. More data, however, are needed to confirm this observation. The major information sources on HPV knowledge and immunization were newspapers and magazines, gynecologists, general practitioners, and pediatricians, whereas internet accounted for less than 2% of the responses. Moreover, 2.5% of the mothers knew about HPV because they had experienced an abnormal Pap-test. The perceived and actual roles of different medical specialists appeared complex. Gynecologists were seen as the most appropriate figure to provide information on HPV infection and immunization, although a significant proportion of mothers identified general practitioners as an appropriate source of information as well. On the other hand, pediatricians were identified as the actual most frequent information providers on HPV immunization. In addition, pediatricians were pointed out as the most preferred medical specialists to carry out vaccination. The preference for pediatricians as immunization providers may be explained by the observation that these specialists are the health care providers for children from birth, opposed to other specialists who are consulted occasionally. Interestingly, a recent survey reported that Italian pediatricians have an insufficient knowledge about HPV although most of those interviewed were in favour of HPV immunization [26]. Public health immunization providers had a more limited role, as they were indicated by less than 10% of mothers as the most appropriate physicians to provide information or to carry out the vaccination. All adolescent girls included in this study had at least one medical encounter with their family pediatrician in the 12 months preceding the interview. Although they were seen by other specialists, none was visited by a gynecologist or by a general practitioner. This result diverges from observations made in the US where adolescents have a less frequent access to primary care [27]. Considering the frequency of contacts, the family pediatrician represents the ideal health provider to recommend immunization in our setting, and the most appropriate specialist to directly inform adolescent girls on HPV infection and HPV immunization. Since mothers are willing to receive information on HPV infection and immunization from gynecologists and general practitioners, these specialists should also actively offer information at every contact with mothers of adolescent girls. Some of the interventions that are proved to be efficacious in improving immunization coverage aim to increase community demand for vaccinations, to enhance access to vaccination services, and to enhance the role of providers [28]. Among potential actions to improve vaccination uptake, mandatory immunization against HPV has been advocated in the US resulting in a strong debate [29,30]. Surveys aimed, as the present study, to investigate determinants of HPV immunization acceptance may help tailoring information and immunization strategies at the local level. Despite having a very high response rate and a large sample that included mothers from all over the country, some limits of the study should be considered. We selected mothers who already participated in other surveys on health problems, who were able to speak Italian, and who had a telephone line. Thus our convenience sample may have selected mothers with a high interest in health issues. This is supported by the finding of a relatively low proportion of mothers who never received Pap-test screening compared with the general population. This may have led to an overestimation of the proportion of mothers with knowledge of HPV and in favour of immunization. In conclusion our study showed that acceptance of HPV immunization is expected to be high in our country and that attitude towards HPV immunization is independent from the level of knowl-
edge of mothers on HPV infection. A strict synergy of family pediatricians, gynecologists, and general practitioners seems desirable to improve information level in families. Since pediatricians have the most frequent contacts with the target population of HPV immunization program, they may also play a key role in providing information to adolescent girls. Acknowledgement This study was supported by an unrestricted grant by Sanofi Pasteur MSD References [1] Brabin L, Roberts SA, Stretch R, Baxter D, Chambers G, Kitchener H, et al. Uptake of first two doses of human papillomavirus vaccine by adolescent schoolgirls in Manchester: prospective cohort study. BMJ 2008;336:1056–8. [2] 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. [3] Garnett GP, Kim JJ, French K, Goldie SJ. Modelling the impact of HPV vaccines on cervical cancer and screening programmes. Vaccine 2006;24:S178–86, s3. [4] Olshen E, Woods ER, Austin SB, Luskin M, Bauchner H. Parental acceptance of the human papillomavirus vaccine. J Adolesc Health 2005;37:248–51. [5] Zimet GD, Liddon N, Rosenthal SL, Lazcano-Ponce E, Allen B. Psychosocial aspects of vaccine acceptability. Vaccine 2006;24:S201–209. [6] Brewer NT, Fazekas KI. Predictors of HPV vaccine acceptability: a theoryinformed, systematic review. Prev Med 2007;45:107–14. [7] Sauvageau C, Duval B, Gilca V, Lavoie F, Ouakki M. Human papilloma virus vaccine and cervical cancer screening acceptability among adults in Quebec, Canada. BMC Public Health 2007;7:304. [8] Constantine NA, Jerman P. Acceptance of human papillomavirus vaccination among Californian parents of daughters: a representative statewide analysis. J Adolesc Health 2007;40:108–15. [9] Marlow LA, Waller J, Wardle J. Parental attitudes to pre-pubertal HPV vaccination. Vaccine 2007;25:1945–52. [10] Lenselink CH, Gerrits MMJG, Melchers WJG, Massuger LFAG, van Hamont D, Bekkers RLM. Parental acceptance of human papillomavirus vaccines. Eur J Obstet Gynecol Reprod Biol 2008;137:103–7. [11] Woodhall SC, Lehtinen M, Verho T, Huhtala H, Hokkanen M, Kosunen E. Anticipated acceptance of HPV vaccination at the baseline of implementation: a survey of parental and adolescent knowledge and attitudes in Finland. J Adolesc Health 2007;40:466–9. [12] Davis K, Dickman ED, Ferris D, Dias JK. Human papillomavirus vaccine acceptability among parents of 10- to 15-year-old adolescents. J Low Genit Tract Dis 2004;8:188–94. [13] Riedesel JM, Rosenthal SL, Zimet GD, Bernstein DI, Huang B, Lan D, et al. Attitudes about human papillomavirus vaccine among family physicians. J Pediatr Adolesc Gynecol 2005:391–8. [14] Kahn JA, Zimet GD, Bernstein DI, Riedesel JM, Lan D, Huang B, et al. Pediatricians’ intention to administer human papillomavirus vaccine: the role of practice characteristics, knowledge, and attitudes. J Adolesc Health 2005;37:502– 10. [15] Raley JC, Followwill KA, Zimet GD, Ault KA. Gynecologists’ attitudes regarding human papilloma virus vaccination: a survey of fellows of the American College of Obstetricians and Gynecologists. Infect Dis Obstet Gynecol 2004;12:127– 33. [16] Duval B, Gilca V, McNeil S, Dobson S, Money D, Gemmill IM, et al. Vaccination against human papillomavirus: a baseline survey of Canadian clinicians’ knowledge, attitudes and beliefs. Vaccine 2007;25:7841–7. [17] Pollack AE, Balkin M, Edouard L, Cutts F, Broutet N, WHO/UNFPA Working Group on Sexual and Reproductive Health and HPV Vaccines. Ensuring access to HPV vaccines through integrated services: a reproductive health perspective. Bull World Health Organ 2007;85:57–63. [18] Kimmel SR. Practical implementation of HPV vaccines in clinical practice. J Fam Pract 2006;1:s18–22. [19] Ciofi Degli Atti ML, Rota MC, Bella A, Salmaso S, ICONA Study Group. Do changes in policy affect vaccine coverage levels? Results of a national study to evaluate childhood vaccination coverage and reasons for missed vaccination in Italy. Vaccine 2004;22:4351–7. [20] National Institute of Statistics. La vita quotidiana nel 2006. ISTAT 2007. [21] Ronco G, Giubilato P, Naldoni C, Zorzi M, Anghinoni E, Scalisi A, et al. Extension of organised cervical cancer screening programmes in Italy and their process indicators. Epidemiol Prev 2007;31:33–47. [22] Di Giuseppe G, Abbate R, Liguori G, Albano L, Angelillo IF. Human papillomavirus and vaccination: knowledge, attitudes, and behavioural intention in adolescents and young women in Italy. Br J Cancer 2008;99:225–9. [23] Noakes K, Yarwood J, Salisbury D. Parental response to the introduction of a vaccine against human papilloma virus. Hum Vaccin 2006;2:243–8. [24] Davis K, Dickman ED, Ferris D, Dias JK. Human papillomavirus vaccine acceptability among parents of 10- to 15-year-old adolescents. J Low Genit Tract Dis 2004:8188–94.
A.E. Tozzi et al. / Vaccine 27 (2009) 2625–2629 [25] Dempsey AF, Zimet GD, Davis RL, Koutsky L. Factors that are associated with parental acceptance of human papillomavirus vaccines: a randomized intervention study of written information about HPV. Pediatrics 2006;117:1486–93. [26] Esposito S, Bosis S, Pelucchi C, Begliatti E, Rognoni A, Bellasio M, et al. Pediatrician knowledge and attitudes regarding human papillomavirus disease and its prevention. Vaccine 2007;25:6437–46. [27] Rand CM, Shone LP, Albertin C, Auinger P, Klein JD, Szilagyi PG. National health care visit patterns of adolescents: implications for delivery of new adolescent vaccines. Arch Pediatr Adolesc Med 2007;161(March (3)):252–9.
2629
[28] Recommendations regarding interventions to improve vaccination coverage in children, adolescents, and adults. Task Force on Community Preventive Services. Am J Prev Med 2000;18:92–6. [29] Alta Charo J. Politics, Parents, and Prophylaxis—Mandating HPV Vaccination in the United States. New Engl J Med 2007;356:1905–8. [30] Haber G, Malow RM, Zimet GD. The HPV vaccine mandate controversy. J Pediatr Adolesc Gynecol 2007;20, 325e331.
Contents lists available at ScienceDirect
Vaccine journal homepage: www.elsevier.com/locate/vaccine
Attitudes towards HPV immunization of Italian mothers of adolescent girls and potential role of health professionals in the immunization program Alberto E. Tozzi ∗ , Lucilla Ravà, D. Stat, Elisabetta Pandolfi, Maria G. Marino, Alberto G. Ugazio Bambino Gesù Hospital, Rome, Italy
a r t i c l e
i n f o
Article history: Received 5 November 2008 Received in revised form 19 January 2009 Accepted 18 February 2009 Available online 24 February 2009 Keywords: HPV vaccine Adolescents Mothers Immunization strategy
a b s t r a c t We assessed the knowledge of Italian mothers of adolescent girls about HPV and HPV vaccination, their willingness to immunize their daughters, and their perception of the role of different medical specialists in the HPV immunization strategy by a telephone interview. Fifty-four percent of the 807 interviewed mothers reported to have ever heard about HPV, and 84% of them were willing to immunize their daughters. Pediatricians most frequently provided information on HPV vaccine (31%), and were perceived as the preferred immunization providers (77%). Acceptance of HPV immunization was high and was not associated with knowledge of HPV. © 2009 Elsevier Ltd. All rights reserved.
1. Introduction The recent implementation of HPV immunization programs in several industrialized countries has resulted so far in a moderate success in terms of vaccination uptake [1,2]. However, since the public health impact of HPV immunization will be greatest if a high coverage of the target population is achieved [3], it is important to identify efficient strategies, suitable for local settings, to maintain and improve HPV immunization coverage. Information strategies are crucial for promoting immunizations. HPV vaccination, however, poses an unusual challenge because it targets female adolescents only and prevents a disease which may occur several decades after immunization, and because related information strategies necessarily touch sensitive issues such as sexual behaviours which parents may be concerned about [4]. Several studies of parental attitudes – mostly carried out in the US – suggest that most parents are in favour of immunizing their children [4–11], although they would need more information [9–11]. Physician recommendation has been considered a strong predictor of vaccine acceptance by parents of girls in the target population [4,12], and several studies have shown that pediatricians, family
∗ Corresponding author at: Bambino Gesù Hospital, Epidemiology Unit, Piazza S. Onofrio 4, 00165 Rome, Italy. Tel.: +39 06 68592401; fax: +39 06 68592853. E-mail address: [email protected] (A.E. Tozzi). 0264-410X/$ – see front matter © 2009 Elsevier Ltd. All rights reserved. doi:10.1016/j.vaccine.2009.02.050
physicians, and gynecologists support HPV immunization [13–16]. Although integration among different health professionals has been recommended in HPV immunization strategies [17,18], studies concerning the attitude towards HPV vaccination have not satisfactorily addressed the parents’ perception of the roles played by specific specialists. In Italy, a local family pediatrician of the National Health System is responsible for delivering primary care until the age of 14. Although most children remain assigned to family pediatricians until this age, families may decide to shift their children to a general practitioner for primary care from the age of 6 years. Other medical specialists of the National Health System, including gynecologists, are consulted in case of need, possibly after an indication by the primary care physician. Immunizations for the general population are delivered in public immunization practices by public health specialists, though 5% of parents opt for immunization in private practices [19]. A national HPV immunization program has recently begun in Italy. In spring 2007 the Ministry of Health started an information campaign that included advertisements on the media and internet web sites. Active offer of HPV immunization to adolescent girls born in 1997 actually started in early 2008. We carried out a cross-sectional study on a large sample of mothers of adolescent girls from all over the country in late 2007, after the information campaign, and before the beginning of the immunization program. Aims of the study were to assess parents’ knowledge about HPV and HPV vaccination and their willingness to have their
2626
A.E. Tozzi et al. / Vaccine 27 (2009) 2625–2629
daughters immunized, and to investigate the roles of the different medical specialists in the immunization strategy as perceived by parents. 2. Methods 2.1. Population and study design We identified as the target population of the study mothers living in any Italian Region with a daughter aged 10–12 years at the time of the interview. Additional eligibility criteria for participation in the study included ability to speak Italian, and availability of a telephone line. For the interview we used a convenience sample of mothers who already participated in other medical surveys and who previously declared their availability to participate in other knowledge, attitude, and practice studies. Mothers were progressively and randomly extracted from a database including 4809 names meeting eligibility criteria until the desired sample size was met, and received a telephone call by a trained operator for the administration of a telephone questionnaire. In case of no answer, a total of three attempts were made to have a successful contact after which the family was withdrawn. Questionnaires were administered from October to December 2007 after obtaining a verbal informed consent. 2.2. Survey questionnaire A 29-item semistructured telephonic questionnaire was used to assess attitudes and knowledge about HPV vaccines, sociodemographic characteristics, and perceived role of medical specialists in providing information and administering HPV vaccine. Some of the answers concerning whom the mothers would prefer their daughters to be vaccinated by, and whom they would prefer as information provider about HPV were open ended and were recoded in categories during the analysis. For these questions the interviewer did not suggest any clue. The interview took approximately 15 min to be completed. 2.3. Sample size and statistical analysis The primary outcomes measured in this study were parental knowledge of HPV and acceptability of HPV vaccines. We calculated that a sample size of 800 mothers would have been sufficient to detect a 50% proportion with knowledge of HPV or willing to accept HPV vaccination for their daughters with a precision of ±4%. Proportions and their 95% confidence intervals were compared through the chi-square test. A multivariate logistic regression analysis was used to determine significant independent predictors of parental knowledge about HPV and acceptability of HPV vaccine. We included in the multivariate analysis sociodemographic variables such as parents’ and child age, parents’ educational level and job, and geographical area of residence. Since it has been suggested that use of Pap-test in mothers may influence their attitude to vaccinate their daughters [6], we also included among independent variables mother’s Pap-test frequency. Finally, we included in the models a variable related to occurrence of child menarche as an indicator of sexual maturity, and the number of visits in the pediatrician’s office in the last 12 months. For the model on attitude towards HPV vaccine, mother’s knowledge of HPV was also included among independent variables. For the purpose of the multivariate analysis, in yes/no/don’t know items, the “no” and “don’t know” answers were grouped together. All data were analyzed using STATA9 (Stata Corp, College Station, TX) statistical software.
3. Results A total of 878 mothers were contacted, and 807 (91.9%) of them accepted to complete the interview. The general characteristics of mothers participating in the study are illustrated in Table 1. Less than one quarter of families included more than one child, more than 15% of the interviewed mothers were single, most parents were white collars, and 53–61% of them had a high school diploma. Our sample showed a slightly higher parent education level compared with the national general population [20]. Less than 10% of the mothers included in the sample never had a Paptest. This frequency was lower than that of the general population [21]. Results concerning knowledge of HPV and HPV immunization are illustrated in Table 2. The level of knowledge of HPV in interviewed mothers was modest: at least one-third stated they had never heard about HPV infection, and only one quarter of respondents declared to have sufficient information about HPV. More than 60% of mothers stated they knew about the national HPV immunization campaign. Interestingly this proportion was slightly higher than that of mothers who declared to have ever heard of human papillomavirus. Among the additional information that interviewed mothers would like to know more about, vaccine safety and efficacy were indicated by 48% and 44% of respondents respectively, while duration of protection was indicated by less than 10% of them. The proportion of mothers willing to accept HPV immunization for their daughters was close to 85%, and cost did not represent a barrier to vaccination since nearly the same proportion of them reported to be ready to pay for having their daughters vaccinated. Mothers who judged positively the immunization program reported prevention of cancer (67.0%) and prevention of a frequent infection (25.1%) as reasons to support HPV vaccination,
Table 1 Characteristics of the 807 interviewed mothers. Mean (S.D.; range) Age of daughters 10 years 11 years 12 years Post-menarchal girls Family with ≥2 children Single parent Mothers’ age Mothers’ educational level (high school diploma) Mothers’ profession Professional White collar Blue collar Housewife Father’s age Fathers’ educational level (high school diploma) Fathers’ profession Professional White collar and army Blue collar Unemployed
N (%) 207 (25.6) 447 (55.4) 153 (19.0) 482 (59.7) 184 (22.8) 133 (16.5)
39.4 (2.4; 31–47) 431 (53.4)
39 (4.8) 433 (53.7) 223 (27.6) 112 (13.9) 43.1 (3.7; 36–54) 494 (61.2)
48 (5.9) 496 (61.5) 212 (26.3) 51 (6.3)
Residency geographic area North Middle South and islands
319 (39.5) 163 (20.2) 325 (40.3)
Mother’s Pap-test frequency Regularly At least once in the life Never
416 (51.5) 326 (40.4) 65 (8.1)
A.E. Tozzi et al. / Vaccine 27 (2009) 2625–2629 Table 2 HPV knowledge and attitude of interviewed mothers.
Only 8.6% of them felt that the vaccine would encourage sexual promiscuity. Table 3 shows the information source on HPV and HPV vaccine reported by interviewed mothers. Newspapers and magazines were the most frequent information source on HPV and HPV immunization. Gynecologists and general practitioners were an information source for HPV in more than 45% of mothers, whereas pediatricians and gynecologists accounted for nearly 41% of the information sources for HPV vaccination. A proportion of 2.5% of the mothers reported they knew HPV because they had experienced an abnormal Pap-test. Radio, television, and the internet were rarely reported as an information source. Table 4 shows the preferred medical specialist by whom mothers would like to be informed on HPV and HPV immunization. Gynecologists were perceived as the preferred source of additional information on both HPV and HPV immunization. The role of general practitioners was also substantial. Although immunizations are not usually provided by pediatricians in Italy, 620 interviewed mothers (76.8%) reported they would prefer them as HPV immunization providers for their daughters, 124 (15.4%) would prefer general practitioners, 58 (7.2%) public health immunization providers, and 5 (0.6%) gynecologists. All daughters of interviewed mothers were visited at least once in a pediatrician office in the 12 months preceding the interview. A total of 267 mothers (33%) declared also that their daughters were visited by other specialists in the previous 12 months. They were most frequently ophthalmologists (27.3%), allergologists (18.0%), and dentists (17.6%). None of the children were seen by a gynaecologist. The multivariate analyses showed that the variables included in the models poorly explained knowledge of HPV infection or HPV immunization acceptance. Knowledge of HPV infection was associated with mother’s age only (OR: 1.1; 95% CI: 1.0–1.2), and HPV immunization acceptance showed no associations with any of the variables included in the model.
N (%) Have you ever heard about human papillomavirus? Yes 437 (54.1) No 270 (33.5) Don’t know 100 (12.4) Would you say you have sufficient information on HPV? Yes 106 (24.3) No 217 (49.7) Don’t know 114 (26.1) Which additional information would you like most to have on HPV vaccine (open ended)? Vaccine safety 387 (48.0) Vaccine efficacy 352 (43.6) Duration of protection 62 (7.7) Other 6 (0.7) Did you know that the Ministry of Health is going to offer an HPV vaccine to 12 years old girls for free? Yes 507 (62.8) No 196 (24.3) Don’t know 104 (12.9) Will you accept the active offer of the HPV vaccine for your daughter? Yes 675 (83.6) No 35 (4.3) Don’t know 97 (12.0) If your daughter was out of the age range for free HPV immunization, would you pay to vaccinate her? Yes 673 (83.4) No 35 (4.3) Don’t know 99 (12.3)
while prevention of genital warts was reported by only 6.4% of supportive mothers. Mothers against the immunization program were concerned about administering too many vaccines (54.3%), and felt that Pap-test was sufficient to prevent cancer (31.4%). Table 3 Information source on HPV and HPV vaccine. Source
4. Discussion N (%)
The results of this study show a good attitude towards HPV vaccination but a definitely poor knowledge level about HPV in the interviewed mothers. The level of knowledge on HPV measured in our study was however higher than that recently reported in a study performed in Italian women [22]. Contrarily to the results of other studies [4,23], less than 10% of the interviewed mothers who were not in favour of HPV immunization feared to encourage sexual promiscuity of their daughters through vaccination, while most of them were worried about the high number of vaccines received. Interestingly, in our study vaccine cost was not perceived as a barrier to immunization, although mothers were informed that cost per dose was approximately 100–120 euros. Only mothers’ age was associated with a better knowledge of HPV, and none of the variables considered in our analysis predicted a positive attitude towards HPV vaccine. Other studies reported contradictory evidence on the efficacy of information strategies on the improvement of the immunization uptake [24,25]. Since knowledge on HPV was not associated with vaccination acceptance,
Who or what was your information source on HPV (open ended)?a Newspapers/magazines 146 (33.4) Gynecologist 116 (26.4) General practitioner 81 (18.5) Friends/relatives 43 (9.8) Radio/TV 32 (7.3) Abnormal Pap-test 11 (2.5) Who or what was your information source on the HPV vaccination program (open ended)?b Newspapers/magazines 193 (38.1) Pediatrician 157 (31.0) Gynecologist 51 (10.1) General practitioner 46 (9.1) Radio/TV 30 (5.9) Friends/relatives 21 (4.1) Internet 9 (1.8) a b
2627
429/437 responses of mothers who had heard about HPV. 507/507 responses of mothers who knew about the vaccination program.
Table 4 Preferred medical specialists for providing information on HPV and HPV immunization.
To which medical specialist would you ask more information on HPV (open ended)? To which medical specialist would you ask more information about HPV immunization (open ended)?
Gynecologist, N (%)
Pediatrician, N (%)
General practitioner, N (%)
Public health immunization provider, N (%)
324 (40.1)
201 (24.9)
242 (30.0)
40 (5.0)
538 (66.7)
5 (0.6)
210 (26.0)
54 (6.7)
2628
A.E. Tozzi et al. / Vaccine 27 (2009) 2625–2629
our findings suggest that improving parents’ knowledge may not increase vaccine acceptability. More data, however, are needed to confirm this observation. The major information sources on HPV knowledge and immunization were newspapers and magazines, gynecologists, general practitioners, and pediatricians, whereas internet accounted for less than 2% of the responses. Moreover, 2.5% of the mothers knew about HPV because they had experienced an abnormal Pap-test. The perceived and actual roles of different medical specialists appeared complex. Gynecologists were seen as the most appropriate figure to provide information on HPV infection and immunization, although a significant proportion of mothers identified general practitioners as an appropriate source of information as well. On the other hand, pediatricians were identified as the actual most frequent information providers on HPV immunization. In addition, pediatricians were pointed out as the most preferred medical specialists to carry out vaccination. The preference for pediatricians as immunization providers may be explained by the observation that these specialists are the health care providers for children from birth, opposed to other specialists who are consulted occasionally. Interestingly, a recent survey reported that Italian pediatricians have an insufficient knowledge about HPV although most of those interviewed were in favour of HPV immunization [26]. Public health immunization providers had a more limited role, as they were indicated by less than 10% of mothers as the most appropriate physicians to provide information or to carry out the vaccination. All adolescent girls included in this study had at least one medical encounter with their family pediatrician in the 12 months preceding the interview. Although they were seen by other specialists, none was visited by a gynecologist or by a general practitioner. This result diverges from observations made in the US where adolescents have a less frequent access to primary care [27]. Considering the frequency of contacts, the family pediatrician represents the ideal health provider to recommend immunization in our setting, and the most appropriate specialist to directly inform adolescent girls on HPV infection and HPV immunization. Since mothers are willing to receive information on HPV infection and immunization from gynecologists and general practitioners, these specialists should also actively offer information at every contact with mothers of adolescent girls. Some of the interventions that are proved to be efficacious in improving immunization coverage aim to increase community demand for vaccinations, to enhance access to vaccination services, and to enhance the role of providers [28]. Among potential actions to improve vaccination uptake, mandatory immunization against HPV has been advocated in the US resulting in a strong debate [29,30]. Surveys aimed, as the present study, to investigate determinants of HPV immunization acceptance may help tailoring information and immunization strategies at the local level. Despite having a very high response rate and a large sample that included mothers from all over the country, some limits of the study should be considered. We selected mothers who already participated in other surveys on health problems, who were able to speak Italian, and who had a telephone line. Thus our convenience sample may have selected mothers with a high interest in health issues. This is supported by the finding of a relatively low proportion of mothers who never received Pap-test screening compared with the general population. This may have led to an overestimation of the proportion of mothers with knowledge of HPV and in favour of immunization. In conclusion our study showed that acceptance of HPV immunization is expected to be high in our country and that attitude towards HPV immunization is independent from the level of knowl-
edge of mothers on HPV infection. A strict synergy of family pediatricians, gynecologists, and general practitioners seems desirable to improve information level in families. Since pediatricians have the most frequent contacts with the target population of HPV immunization program, they may also play a key role in providing information to adolescent girls. Acknowledgement This study was supported by an unrestricted grant by Sanofi Pasteur MSD References [1] Brabin L, Roberts SA, Stretch R, Baxter D, Chambers G, Kitchener H, et al. Uptake of first two doses of human papillomavirus vaccine by adolescent schoolgirls in Manchester: prospective cohort study. BMJ 2008;336:1056–8. [2] 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. [3] Garnett GP, Kim JJ, French K, Goldie SJ. Modelling the impact of HPV vaccines on cervical cancer and screening programmes. Vaccine 2006;24:S178–86, s3. [4] Olshen E, Woods ER, Austin SB, Luskin M, Bauchner H. Parental acceptance of the human papillomavirus vaccine. J Adolesc Health 2005;37:248–51. [5] Zimet GD, Liddon N, Rosenthal SL, Lazcano-Ponce E, Allen B. Psychosocial aspects of vaccine acceptability. Vaccine 2006;24:S201–209. [6] Brewer NT, Fazekas KI. Predictors of HPV vaccine acceptability: a theoryinformed, systematic review. Prev Med 2007;45:107–14. [7] Sauvageau C, Duval B, Gilca V, Lavoie F, Ouakki M. Human papilloma virus vaccine and cervical cancer screening acceptability among adults in Quebec, Canada. BMC Public Health 2007;7:304. [8] Constantine NA, Jerman P. Acceptance of human papillomavirus vaccination among Californian parents of daughters: a representative statewide analysis. J Adolesc Health 2007;40:108–15. [9] Marlow LA, Waller J, Wardle J. Parental attitudes to pre-pubertal HPV vaccination. Vaccine 2007;25:1945–52. [10] Lenselink CH, Gerrits MMJG, Melchers WJG, Massuger LFAG, van Hamont D, Bekkers RLM. Parental acceptance of human papillomavirus vaccines. Eur J Obstet Gynecol Reprod Biol 2008;137:103–7. [11] Woodhall SC, Lehtinen M, Verho T, Huhtala H, Hokkanen M, Kosunen E. Anticipated acceptance of HPV vaccination at the baseline of implementation: a survey of parental and adolescent knowledge and attitudes in Finland. J Adolesc Health 2007;40:466–9. [12] Davis K, Dickman ED, Ferris D, Dias JK. Human papillomavirus vaccine acceptability among parents of 10- to 15-year-old adolescents. J Low Genit Tract Dis 2004;8:188–94. [13] Riedesel JM, Rosenthal SL, Zimet GD, Bernstein DI, Huang B, Lan D, et al. Attitudes about human papillomavirus vaccine among family physicians. J Pediatr Adolesc Gynecol 2005:391–8. [14] Kahn JA, Zimet GD, Bernstein DI, Riedesel JM, Lan D, Huang B, et al. Pediatricians’ intention to administer human papillomavirus vaccine: the role of practice characteristics, knowledge, and attitudes. J Adolesc Health 2005;37:502– 10. [15] Raley JC, Followwill KA, Zimet GD, Ault KA. Gynecologists’ attitudes regarding human papilloma virus vaccination: a survey of fellows of the American College of Obstetricians and Gynecologists. Infect Dis Obstet Gynecol 2004;12:127– 33. [16] Duval B, Gilca V, McNeil S, Dobson S, Money D, Gemmill IM, et al. Vaccination against human papillomavirus: a baseline survey of Canadian clinicians’ knowledge, attitudes and beliefs. Vaccine 2007;25:7841–7. [17] Pollack AE, Balkin M, Edouard L, Cutts F, Broutet N, WHO/UNFPA Working Group on Sexual and Reproductive Health and HPV Vaccines. Ensuring access to HPV vaccines through integrated services: a reproductive health perspective. Bull World Health Organ 2007;85:57–63. [18] Kimmel SR. Practical implementation of HPV vaccines in clinical practice. J Fam Pract 2006;1:s18–22. [19] Ciofi Degli Atti ML, Rota MC, Bella A, Salmaso S, ICONA Study Group. Do changes in policy affect vaccine coverage levels? Results of a national study to evaluate childhood vaccination coverage and reasons for missed vaccination in Italy. Vaccine 2004;22:4351–7. [20] National Institute of Statistics. La vita quotidiana nel 2006. ISTAT 2007. [21] Ronco G, Giubilato P, Naldoni C, Zorzi M, Anghinoni E, Scalisi A, et al. Extension of organised cervical cancer screening programmes in Italy and their process indicators. Epidemiol Prev 2007;31:33–47. [22] Di Giuseppe G, Abbate R, Liguori G, Albano L, Angelillo IF. Human papillomavirus and vaccination: knowledge, attitudes, and behavioural intention in adolescents and young women in Italy. Br J Cancer 2008;99:225–9. [23] Noakes K, Yarwood J, Salisbury D. Parental response to the introduction of a vaccine against human papilloma virus. Hum Vaccin 2006;2:243–8. [24] Davis K, Dickman ED, Ferris D, Dias JK. Human papillomavirus vaccine acceptability among parents of 10- to 15-year-old adolescents. J Low Genit Tract Dis 2004:8188–94.
A.E. Tozzi et al. / Vaccine 27 (2009) 2625–2629 [25] Dempsey AF, Zimet GD, Davis RL, Koutsky L. Factors that are associated with parental acceptance of human papillomavirus vaccines: a randomized intervention study of written information about HPV. Pediatrics 2006;117:1486–93. [26] Esposito S, Bosis S, Pelucchi C, Begliatti E, Rognoni A, Bellasio M, et al. Pediatrician knowledge and attitudes regarding human papillomavirus disease and its prevention. Vaccine 2007;25:6437–46. [27] Rand CM, Shone LP, Albertin C, Auinger P, Klein JD, Szilagyi PG. National health care visit patterns of adolescents: implications for delivery of new adolescent vaccines. Arch Pediatr Adolesc Med 2007;161(March (3)):252–9.
2629
[28] Recommendations regarding interventions to improve vaccination coverage in children, adolescents, and adults. Task Force on Community Preventive Services. Am J Prev Med 2000;18:92–6. [29] Alta Charo J. Politics, Parents, and Prophylaxis—Mandating HPV Vaccination in the United States. New Engl J Med 2007;356:1905–8. [30] Haber G, Malow RM, Zimet GD. The HPV vaccine mandate controversy. J Pediatr Adolesc Gynecol 2007;20, 325e331.