Preventive Medicine 64 (2014) 69–74

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Human papillomavirus vaccine acceptability among parents of adolescent girls: Obstacles and challenges in Mysore, India Purnima Madhivanan a,b,⁎, Tan Li a, Vijaya Srinivas b, Laura Marlow c, Soumyadeep Mukherjee a, Karl Krupp a,b a b c

Robert Stempel College of Public Health and Social Work, Florida International University, Miami, USA Public Health Research Institute of India, Mysore, India Health Behavior Research Centre, Department of Epidemiology and Public Health, UCL, London, UK

a r t i c l e

i n f o

Available online 13 April 2014 Keywords: Acceptability Adolescent Barrier Correlate India Human papillomavirus School Vaccine

a b s t r a c t Objective. Worldwide, 530,000 women are diagnosed with cervical cancer and 275,000 die annually. India bears the greatest burden of the disease with 132,000 cases and 74,000 deaths yearly. Widespread uptake of human papillomavirus (HPV) vaccine could reduce incidence and mortality by two-thirds. This study explored obstacles and facilitators of parental acceptability of HPV vaccine. Methods. In 2010, questionnaires were sent home with a random sample of 800 girls attending 12 schools in Mysore city to be completed by a parent. Data were analyzed using multivariable logistic regression with generalized estimating equation to account for potential clustering by school. Results. Of the 797 completed surveys; 71% reported willingness to accept HPV vaccine for their daughters. The adjusted odds of acceptance was higher among participants who received recommendation from their parents, perceived cervical cancer as a serious disease, believed that HPV vaccine was safe, or felt that vaccination was a good way to protect against cervical cancer. Parents who had concerns about vaccine side-effects or thought that it would cause pain had lower odds of acceptance. Conclusion. Future promotion of vaccine should emphasize safety of immunization and involve promotion to the extended family, so that they actively recommend immunization of young adolescent girls. © 2014 Published by Elsevier Inc.

Introduction Since its introduction in 2006, more than 79 million doses of the human papillomavirus (HPV) vaccine have been administered worldwide (Sane Vax Inc. letter concerning gardasil [Internet], 2011). The vast majority of these immunizations have been in the United States (46 million), Australia (6 million), United Kingdom (5 million) and other developed countries (Canfell et al., 2006; Downs et al., 2008; HPV vaccination [Internet], 2012; HPV vaccine — questions &, answers [Internet], 2012; World Health Organization, 2012). Adoption in low-resource settings, where eight of every ten cervical cancer deaths occur, has been more slow (Cohen, 2007; Cervical cancer, human papillomavirus (HPV), HPV vaccines, 2007), which is partially due to the high cost of HPV vaccine (Fernández et al., 2010). Public awareness and knowledge about the HPV and cervical cancer are also low in the

Abbreviations: HPV, Human Papillomavirus; NGO, Non-governmental Organization; OR, Odds Ratio; CI, Confidence Interval. ⁎ Corresponding author at: Department of Epidemiology, Robert Stempel College of Public Health and Social Work, 11200 SW 8 Street, HLS 390W2, Miami, FL 33199, USA. Fax: +1 305 348 4901. E-mail address: pmadhiva@fiu.edu (P. Madhivanan).

http://dx.doi.org/10.1016/j.ypmed.2014.04.002 0091-7435/© 2014 Published by Elsevier Inc.

developing world (Alsaad et al., 2012). In India, little is known about the obstacles and facilitators of HPV immunization among parents of adolescent girls. This is consistent with the findings of a 2010 systematic review of HPV vaccine acceptability that found few quantitative studies had been carried out in developing countries where cervical cancer is most prevalent (Allen et al., 2010). India has the highest burden of cervical cancer in the world, with about one-fifth of all cases. Annually, approximately 132,000 women are diagnosed with the disease, and 74,000 die (Verma and Khanna, 2013). According to a 2012 study, cervical cancer is now the most common cause of cancer death among Indian women, accounting for 17% of all cancer mortality (Dikshit et al., 2012). Unlike the United States and Europe, population-based Pap smear screening has not been implemented due to the shortage of laboratory facilities and expert cytologists (Vedantham et al., 2010). As a consequence, the risk of a woman dying from cervical cancer in India has now overtaken her risk of dying during child birth (0.7% vs. 0.6% respectively) (Dikshit et al., 2012; World Health Organization et al., 2012). The lack of screening programs to identify and treat women with cervical cancer in India has given added public health impetus to primary prevention using vaccines that target oncogenic strains of the HPV (Kaarthigeyan, 2012). Two prophylactic HPV vaccines, Gardasil and Cervirax were approved in 2006 by the Drug Controller General of

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India for girls and women aged 9 to 26 (Singhal et al., 2008). During the same year PATH, an international nongovernmental organization (NGO), embarked on a 5-year HPV vaccine demonstration program, that eventually resulted in a controversy when seven HPV-vaccinated tribal girls died in 2010 (Srinivasan, 2011). Data for this study was collected during the same period in Karnataka, although there was no evidence that the negative news coverage from the PATH study affected the acceptability of HPV vaccine among parents (Feinberg, 2010). In studies from other parts of the world, parental acceptability for immunizing against HPV ranged from 54.9% to 81.0% (Tricco et al., 2007). Parental acceptance was higher if a physician recommended immunization; if parents thought that the consequences of infection were severe, the vaccine was effective, or that their child was at-risk for HPV infection or cancer. They reported higher acceptability if they knew someone with cancer (Brewer and Fazekas, 2007; Sam et al., 2009; Trim et al., 2011). Obstacles to immunizing adolescent girls included concerns about vaccine safety and its potential side effects. High cost and concerns about immunization promoting adolescent sexual behavior were also barriers to vaccination (Bartolini et al., 2012; Becker-Dreps et al., 2010; Brewer and Fazekas, 2007; Sam et al., 2009). While few difference in attitudes toward HPV vaccination have been found between urban and rural parents in the developed world (El-Khatiba et al., 2012), research from Botswana and India showed that people living outside of cities expressed more positive attitudes towards vaccinating their daughters against HPV than their urban counterparts (DiAngi et al., 2011; Madhivanan et al., 2009). Based on a previous qualitative study on the HPV vaccine among urban parents in the same population (Madhivanan et al., 2009), we hypothesized that acceptability of HPV immunization of adolescent daughters would be relatively high. This paper reports findings from a quantitative survey exploring predictors of HPV vaccine acceptability among a random sample of parents of adolescent school-going girls in urban Mysore, India. Method Study setting Between February and December 2010, the study was carried out by the Public Health Research Institute of India (PHRII) in the city of Mysore, India. Mysore is the second largest city in the southern state of Karnataka with a population of 887,446 of which 443,633 are female (Census, 2011 [Internet], 2011). Schools The schools selected for the survey were chosen to capture the demographic diversity of families living in the city. A cluster of 12 schools were selected with probability-proportionate-to-size (PPS) to ensure representativeness of the sample. These included five government schools, three religious schools, and four private schools located in a variety of settings from center-city Mysore, urban and peri-urban neighborhoods. Permission was first sought from the Block Education Officer to conduct the study in the schools. Subsequently, the administration of each of the selected schools was contacted and solicited for participation. Participants Parents were included in the study if they had at least one adolescent (ages 11–15) daughter attending a participating school, were able to speak and understand English or Kannada, the local language; and were able to give informed consent. A program announcement was first sent home with all girls attending 7th through 10th grades that explained the study and invited eligible parents to participate. The research team then systematically enumerated all girls in the target age group in the selected schools, and from that sampling frame, selected a simple random sample of 800 female students. A flyer explaining the study and inviting parents to participate was sent home with the chosen students. Students were asked to return the form the next day with a parental signature and phone number if their parents were interested to hear more about the study. Potential participants were subsequently contacted by phone by a trained

recruiter. The recruiter assessed their interest in the study and collected demographic information allowing researchers to examine differences between parents who elected to participate, and those who did not. Procedures A package containing one self-administered questionnaire in English and Kannada, an informed consent form, an information sheet about cervical cancer and prevention, and a pen was sent home with all girls whose parents had indicated that they were willing to complete a survey. All the students were given instructions to return the completed questionnaire to the school within seven days. If the questionnaire was not returned in the prescribed time, study staff made a reminder phone call to parents about the survey. The study was approved by the Institutional Review Board of the Public Health Research Institute of India (Protocol # 2009-04-19-04) and Florida International University (IRB-13-0022). Measures Questionnaires covered the following topics: knowledge about HPV infection and cervical cancer, beliefs about perceived benefits and barriers to vaccination, perceptions about whether their daughter might be at-risk for HPV infection, beliefs concerning the severity of HPV-related diseases including cervical cancer, and questions about parental informational needs in relation to the HPV vaccination. Intention-to-vaccinate was operationalized with the question: ‘If your daughter were invited to get an HPV vaccination, would you agree to her having it sometime soon?’ Parents could respond on a 4-point scale (definitely not, probably not, yes probably, and yes definitely). Measures used in the study were based on the Health Belief Model, Social Cognition Theory, and previous HPV vaccine acceptance research conducted by our group (Brewer and Fazekas, 2007; Glanz et al., 2008; Kohler et al., 1999; Krupp et al., 2010; Madhivanan et al., 2009; Marlow et al., 2007; Waller et al., 2006). Our approach was to focus on factors that would affect parental perceptions about risk and severity of HPV-related disease, benefits and risks of immunization, and cues-to-action. These included knowledge and perceptions about government vaccination programs, cultural attitudes and beliefs about immunization, and parental beliefs about vaccination in general, and HPV-vaccination specifically. Participants were also asked if they had any personal experience of cancer in their family or close friends, and whether they had ever heard of HPV. Perceived severity of HPV and susceptibility to HPV were measured using terms from a scale developed by Witte et al. (Witte, 1996) (e.g. ‘I believe that HPV can be serious’; ‘It is likely that my daughter will get HPV one day’), rated on a three-point scale from disagree to agree. Both scales showed good internal reliability within this sample (Cronbach's alpha = 0.78 and 0.70 respectively). Four items assessed perceived barriers and benefits in relation to vaccination generally. All items are listed in Table 2. They include favorable items (e.g. ‘having the vaccination would be a good way to protect my daughter against cervical cancer’) and unfavorable items (e.g. ‘having the HPV vaccination might make girls more likely to have sex’). Vaccine-general items included ‘I don't want to give my daughter too many vaccinations’. These were measured using three-point scales (agree, disagree, and not sure). Participants were then asked to read a brief information sheet about HPV vaccination before completing the section on perceived benefits and risks of HPV vaccination [included as Appendix A]. Most items were adapted from instruments used in previous studies on HPV vaccine acceptability (Krupp et al., 2010; Madhivanan et al., 2009) and studies conducted among southeast Asians living in the UK (Marlow et al., 2009). Social norms were assessed by respondent's beliefs whether their doctor, husband, parents or in-laws, and friends would find HPV vaccination acceptable. In each case they were asked to indicate whether target persons ‘would rather I vaccinate’, ‘wouldn't mind whether I vaccinated’ or ‘would rather I did not vaccinate’. Data analysis Data were analyzed using Stata 10.1 (Stata Corporation, College Station, TX) and SAS 9.2 (SAS Institute Inc., Cary, North Carolina, USA). Descriptive statistics were used to provide a general profile of the study population. ‘Intention-tovaccinate’ was dichotomized; participants who indicated ‘yes probably’ or ‘yes definitely’ were classified as ‘acceptors’ and those indicating ‘probably not’ or ‘definitely not’ or ‘not sure’ were classified as ‘non-acceptors’ (Marlow et al., 2007). Bivariate associations between vaccine acceptability and predictor variables were assessed using the Pearson chi-squared test or Fisher exact

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test. Variables with two tailed p-values less than 0.05 were considered for inclusion in a multivariable logistic regression model to establish whether the predictor variables were associated with acceptance of HPV vaccination. Individuals with missing data were excluded only from analysis of those items. Confidence intervals were calculated at the 95% level. To evaluate the relationship between acceptability of HPV vaccine and socio-demographics and other factors, odds ratios (ORs) and 95% confidence intervals were estimated using logistic regression with a generalized estimating equation (PROC GENMOD in SAS) to account for potential clustering by school in the analyses.

Results Of the 800 survey packets distributed to parents, 797 were completed (99.6%). Of these, 19 (2.3%) were excluded from the analyses because they were returned without a signed consent form. About 64% of the participants were less than 40 years old, 19% were Muslims, 15% had no education and 69% were mothers (Table 1). Parental acceptability of HPV vaccination Five hundred fifty-six (71.5%) parents said they would ‘probably’ or ‘definitely’ accept HPV vaccination for their daughter, and 28.5% said

Table 1 Relationship of demographic and psychosocial characteristics associated with parental HPV vaccination acceptability in Mysore City, India in 2010 (N = 778). Characteristic

Respondent age ≤35 yrs 36–40 yrs 41–45 yrs ≥46 yrs Education level None 1st to 10th grade High School & Bachelor's Degree Master's degree or above Vocational training (Diploma) Religion Other religions Muslim Employment status Employed full time Employed part-time Self-employed Full time home maker Retired/Unemployed Respondent Father Mother Heard of HPV before Yes No Experience of cancer Yes No Vaccination recommended byc Doctor Spouse Friends Your parents Other relatives Your in-laws Your neighbors

Acceptability of HPV vaccine N

%a

n

%b

Unadj OR 95% CI

242 257 157 122

31.1 33.0 20.2 15.7

190 192 118 91

78.5 74.7 75.2 74.6

1.00 0.82 0.83 0.81

0.60, 1.12 0.50, 1.38 0.40, 1.66

116 14.9 394 50.6 189 24.3 39 5.0 40 5.1

93 297 142 29 30

80.2 75.4 75.1 74.4 75.0

1.00 0.77 0.77 0.80 0.88

0.56, 1.07 0.47, 1.25 0.27, 2.41 0.37, 2.09

632 81.2 146 18.8

495 77.9 1.00 96 65.8 1.12

0.41, 3.03

214 83 112 339 30

159 67 82 263 20

1.00 1.25 0.89 1.28 0.32

0.69, 2.29 0.59, 1.34 0.96, 1.72 0.23, 1.70

241 31.0 537 69.0

179 74.3 1.00 412 76.7 1.26

0.83, 1.91

221 28.4 557 71.6

177 80.1 1.26 414 74.3 1.00

0.82, 1.95

158 20.3 620 79.7

131 82.9 1.67 460 74.2 1.00

1.03, 2.73

506 298 206 404 194 236 190

432 268 181 346 172 209 170

2.86, 5.14 2.98, 5.35 1.88, 3.62 1.99, 4.08 1.77, 4.63 2.00, 4.65 2.10, 4.84

27.5 10.7 14.4 43.6 3.9

65.0 38.30 23.48 51.93 24.94 30.33 24.42

74.3 80.7 73.2 77.6 66.7

85.4 89.9 87.9 85.6 88.7 88.6 89.5

3.83 3.99 2.61 2.85 2.86 3.05 3.18

Note: When the expected cell frequency was smaller than 5, Fisher's Exact Test was performed to test for statistical significance; Unadj OR = Unadjusted Odds Ratio; 95% CI = 95% Confidence Intervals; p b 0.05 is considered statistically significant. a Percentage for each category out of the total (N = 778). b Percentage of HPV vaccine acceptability among parents within each category. c No is the referent category.

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they ‘probably’ or ‘definitely’ not consider immunizing their daughter with HPV vaccine.

Parental attitudes and beliefs about HPV, cervical cancer and HPV vaccination Table 2 describes attitudes and beliefs associated with parental acceptance of the HPV vaccine. A majority of the parents believed that HPV could cause serious health problems (74.2%) and cervical cancer would be extremely harmful (79.3%). Most participants (91.4%) believed that HPV vaccination was a good way to protect their daughter against cervical cancer. While a vast majority of respondents (92.8%) thought that the vaccine was safe, 31.6% were concerned about possible side-effects. About 73.8% of parents thought there wasn't enough information available about the HPV vaccine, 30.1% said that the cost of the immunization was too high and 45.5% were concerned that vaccinating against HPV might make girls more likely to have sex. About 1 in 5 respondents (20%) knew someone with cancer; 83% of these respondents indicated they would immunize their daughters against HPV infection.

Determinants of HPV vaccine acceptability Participants reporting that they knew someone with cancer had higher (Odds Ratio [OR]:1.67; 95% CI: 1.03, 2.73; p = 0.03) odds of finding the vaccine acceptable, compared to participants who did not know someone with cancer (Table 1). Higher perceived severity and susceptibility of cervical cancer were associated with acceptability of HPV vaccination (Table 2). Participants who believed in general and specific vaccination benefits had higher odds of reporting that they would vaccinate their daughter. Participants believing HPV infection as extremely harmful had higher odds of accepting HPV vaccination compared to participants who did not. Those who believed that cervical cancer was a serious disease also had higher odds of vaccinating their daughters (OR: 2.52; 95% CI: 1.61, 3.94; p b 0.0001). Those who believed that the HPV vaccine was safe; or was a good way to protect their daughter against cervical cancer had higher odds of accepting the vaccine. Factors independently associated with increased odds of HPV vaccine acceptance in the multivariable logistic regression analyses included belief that cervical cancer was a serious disease; that the HPV vaccine was safe; and that vaccination was a good way to protect their daughter against cervical cancer. Concerns about vaccine side effects and pain were associated with lower adjusted odds of HPV vaccine acceptability (Table 3).

Discussion This study is the first to evaluate parental acceptability of HPV vaccination among a randomly selected sample of parents of adolescent girls in south India. Our survey found that 71.5% of parents were willing to vaccinate their daughters, a rate that falls in the high end of the 54.9% to 81% range found across the world (Census, 2011 [Internet], 2011). Belief in the vaccine's safety and efficacy increased the odds of accepting vaccination. Believing that parents would favor the vaccine also increased the odds that study participants would accept the vaccine for their daughters. Perceived susceptibility and severity were found to be predictive of HPV vaccine acceptability. In vaccination programs, cues-to-action such as messages about the safety and efficacy of HPV immunization were particularly important in parental decisions about vaccinating daughters. Since believing that a parent would approve of vaccination increased the odds of acceptability, marketing the vaccine to extended family members appears to be a promising strategy to increase its uptake.

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Table 2 Relationship of attitudes and beliefs associated with parental HPV Vaccine acceptability for adolescent daughters attending schools in Mysore City, India in 2010 (N = 778). Itemsa

Severity I believe the HPV can be extremely harmful. I believe that HPV can cause serious health problems. I believe that cervical cancer can be extremely harmful. I believe that cervical cancer is a serious disease. Susceptibility It is likely that my daughter will get HPV in the future.d My daughter may be at-risk of getting HPV infection.d It is possible that my daughter will get cervical cancer in the future.d It is likely that my daughter may get cervical cancer someday.d Barriers General I am concerned about side effects of vaccinations. I am afraid of vaccinating my children. I would feel responsible if anything bad happened because I had my child vaccinated. Vaccine specific Worry that daughter may become sexually active Having the HPV vaccination might make girls more likely to have sex.d High cost of the vaccine Injection may cause pain Not enough information available about the vaccine Worried about safety of the vaccine Benefits General Vaccines are effective at preventing diseases. It is very important that my daughter receive all her vaccinations. It is better to get the disease and get protected from it naturally than to be vaccinated.e Vaccination is one way that parents can ensure their child's health. Vaccine specific Having the vaccination would be a good way to protect daughter against cervical cancer. Believe that HPV vaccine is safe.

Acceptability of HPV vaccine N

%b

n

%c

586 577 617 612

75.3 74.2 79.3 78.7

478 473 491 491

81.6 81.9 83.1 80.2

2.65 3.47 1.42 2.52

1.40, 5.01 1.98, 6.09 0.74, 2.72 1.61, 3.94

123 128 125 118

15.8 16.5 16.1 15.2

94 94 100 91

76.4 73.4 80.0 77.2

1.31 1.07 2.12 1.47

0.78, 2.22 0.66, 1.74 1.24, 3.63 1.09, 2.32

246 131 306

31.6 16.8 39.3

178 80 234

72.4 61.1 76.5

0.67 0.41 1.03

0.48, 0.92 0.16, 1.03 0.81, 1.31

354 144 430 339 563 580

45.5 18.5 55.3 44.4 73.8 75.5

288 119 329 233 443 457

81.4 82.6 76.5 68.7 78.7 78.8

1.87 1.19 1.07 0.48 1.48 1.83

1.29, 2.69 0.68, 2.10 0.80, 1.43 0.30, 0.76 1.08, 2.04 1.04, 3.24

618 736 333 738

79.4 94.6 42.8 94.9

484 573 280 574

78.3 77.8 84.1 77.8

1.48 2.76 2.05 3.08

0.84, 2.62 1.06, 7.21 1.73, 2.42 1.31, 7.25

700 717

91.4 92.8

561 575

80.1 80.2

5.78 11.45

3.06, 10.93 4.72, 27.79

Unadj OR

95% CI

Note: When the expected cell frequency was smaller than 5, Fisher's Exact Test was performed to test for statistical significance; Unadj OR = Unadjusted Odds Ratio; 95% CI = 95% Confidence Intervals; p b 0.05 is considered statistically significant. a No is the referent category. b Percentage for each category out of the total (N = 778). c Percentage of HPV vaccine acceptability among parents within each category. d Variables couldn't be fitted in GEE (logistic regression with correlated individuals, PROC GENMOD in SAS) since there were missing values for some schools. The variables were fitted in regular logistic regression. e Item value reversed.

Table 3 Determinants of HPV vaccine acceptability among a random sample of parents of adolescent school going girls in Mysore City, India in 2010 (N = 778) using multivariable logistic regression. Itemsa

Marital status Experience of cancer Vaccine recommended by doctor Vaccine recommended by spouse Vaccine recommended by friends Vaccine recommended by your parents Vaccine recommended by other relatives Vaccine recommended by your in-laws Vaccine recommended by your neighbors I believe that HPV can be extremely harmful. I believe that HPV can cause serious health problems. I believe that cervical cancer is a serious disease. I am concerned about side effects of vaccinations. Worry that daughter may become sexually active Injection may cause pain. Not enough information available about the vaccine Worried about safety of the vaccine It is very important that my daughter receive all her vaccinations. It is better to get the disease and get protected from it naturally than to be vaccinated.c Vaccination is one way that parents can ensure their child's health. Having the vaccination would be a good way to protect daughter against cervical cancer. Believe that HPV vaccine is safe p b 0.05 is considered statistically significant. a No is the referent category. b OR adjusted for all other variables in the model. c Item value reversed.

Acceptability of HPV vaccineb adj OR

95% CI

1.23 1.25 1.14 1.67 0.62 2.41 0.93 1.60 1.63 1.90 2.86 3.14 0.53 1.12 0.32 0.86 1.65 2.55 0.83 1.54 8.95 10.88

0.40, 3.81 0.67, 2.33 0.58, 2.34 0.88, 3.18 0.26, 1.48 1.47, 3.96 0.43, 2.04 0.41, 6.21 0.79, 3.38 0.39, 9.27 0.61, 13.29 1.08, 9.05 0.30, 0.92 0.58, 2.17 0.16, 0.67 0.45, 1.64 0.42, 5.88 0.19, 34.74 0.54, 1.26 0.19, 12.28 3.15, 25.45 2.84, 41.71

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Study limitations and strengths This study had several limitations. It utilized a sample of parents of school-going adolescents, so findings may not be representative of the population as a whole. Additionally, even among parents of schoolgoing children, certain segments of the population may not have been represented in the selected institutions. An anonymous questionnaire should have allowed parents to respond more accurately to sensitive questions. Individuals reporting no education may have received help from their spouse or extended family to complete the survey. Because information about cervical cancer and prevention was included in the same packet as the survey, it is possible that the parent's belief about HPV and cervical cancer could have been influenced by the information provided. This study measured stated acceptance of HPV vaccination, which may not reflect actual uptake. Despite these limitations, our study has important strengths. We examine acceptability of HPV vaccination using a theoretical framework and a large random sample of participants. The response rate was high, with little missing data. We also utilized a tested survey instrument making it possible to compare findings across populations. Conclusion Our study presents an encouraging view of parental acceptance of HPV vaccination similar to another study conducted in Northern India (Basu and Mittal, 2011). Future promotion of vaccine should emphasize the safety of vaccines and involve extended family to actively recommend immunization of young adolescent Indian girls. Implications and contribution This is the first study to examine HPV vaccine acceptability among a random sample of Indian parents with adolescent daughters. It presents an encouraging picture with 71% of parents willing to immunize their daughter. Perceptions of vaccine safety and acceptance by extended family members influenced parental decisions to vaccinate. Brief description of the novelty and impact of the work This is the first HPV vaccine acceptability study carried out in a random sample of Indian parents of adolescent girls. It presents an encouraging picture of acceptance of this important vaccine. About 71% of parents would consider immunizing their daughter. There was little evidence that socio-demographic factors influenced vaccine acceptance. Future promotional messages should emphasize vaccine safety and acceptance by extended family members since both factors figured heavily in parental decisions about vaccine acceptance. Conflict of interests The authors declare that they have no competing interests.

Authors' contributions PM, KK and LM were involved in the conception and design of the study. VS, PM and KK were responsible for acquisition of data. PM, TL and SM analyzed the data. PM, SM and KK drafted the article and all authors (PM, TL, VS, LM, SM, KK) participated in interpreting the data and critically revising the manuscript for important intellectual content. All authors read and approved the final version of the manuscript to be published. Previous presentations Partial results from this study were presented at the 6th Annual Society for Epidemiological Research Meeting held in Boston from 18

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to 21 June 2013 and the STI & AIDS World Congress 2013 (Joint Meeting of the 20th ISSTDR and 14th IUSTI Meeting) held in Vienna from 14 to 17 July 2013. Acknowledgments For their generous assistance on this project, the authors would like to thank the Block Development Officer for Mysore, the administrative staff of the schools involved for their help and the parents who took the time to complete the questionnaires. Sincere thanks to Savitha Gowda, Fazila Begum and Poornima Jaykrishna from PHRII for their tremendous help in carrying out this study. The authors appreciate the statistical support by Ahmed N. Albatineh from Florida International University. The study was funded by Investigator Initiated Award from Merck & Co., Inc. Merck had no role in the study design, conduct, collection, management, analysis, or interpretation of the data, or preparation, review, or approval of the manuscript. Appendix A. Supplementary data Supplementary data to this article can be found online at http://dx. doi.org/10.1016/j.ypmed.2014.04.002. References Allen, J.D., Coronado, G.D., Williams, R.S., et al., 2010. A systematic review of measures used in studies of human papillomavirus (HPV) vaccine acceptability. Vaccine 28 (24), 4027–4037. Alsaad, M.A., Shamsuddin, K., Fadzil, F., 2012. Knowledge towards HPV infection and HPV vaccines among Syrian mothers. Asian Pac. J. Cancer Prev. 13, 879–883. Bartolini, R.M., Winkler, J.L., Penny, M.E., LaMontagne, D.S., 2012. Parental acceptance of HPV vaccine in Peru: a decision framework. PLoS ONE 7 (10), e48017. Basu, P., Mittal, S., 2011. Acceptability of human papillomavirus vaccine among the urban, affluent and educated parents of young girls residing in Kolkata, Eastern India. J. Obstet. Gynaecol. Res. 37 (5), 393–401. Becker-Dreps, S., Otieno, W.A., Brewer, N.T., Agot, K., Smith, J.S., 2010. HPV vaccine acceptability among Kenyan women. Vaccine 28 (31), 4864–4867. Brewer, N.T., Fazekas, K.I., 2007. Predictors of HPV vaccine acceptability: a theoryinformed, systematic review. Prev. Med. 45 (2), 107–114. Canfell, K., Sitas, F., Beral, V., 2006. Cervical cancer in Australia and the United Kingdom: comparison of screening policy and uptake, and cancer incidence and mortality. Med. J. Aust. 185 (9), 482. Census 2011 [Internet], 2011. Available from: http://censusindia.gov.in/. Cervical cancer, human papillomavirus (HPV), HPV vaccines, 2007. Key points for policymakers and health professionals [Internet]. Available from: www.searo.who.int/ LinkFiles/Publications_Cervical_Cancer_HPV.pdf. Cohen, S.A., 2007. A long and winding road: getting the HPV vaccine to women in the developing world. Guttmacher Policy Rev. 10 (3). DiAngi, Y.T., Panozzo, C.A., Ramogola-Masire, D., Steenhoff, A.P., Brewer, N.T., 2011. A cross-sectional study of HPV vaccine acceptability in Gaborone, Botswana. PLoS ONE 6 (10), e25481. Dikshit, R., Gupta, P.C., Ramasundarahettige, C., et al., 2012. Cancer mortality in India: a nationally representative survey. Lancet 379 (9828), 1807–1816. Downs, L.S., Smith, J.S., Scarinci, I., Flowers, L., Parham, G., 2008. The disparity of cervical cancer in diverse populations. Gynecol. Oncol. 109 (2), S22–S30. El-Khatiba, Z., Tota, J.E., Kaufmann, A.M., 2012. Progress on human papillomavirus (HPV) infection and cervical cancer prevention in sub-Saharan Africa: highlights of the 27th International Papillomavirus Conference in Berlin, 17–22 September 2011. J. Epidemiol. Glob. Health 2 (2), 99–102. Feinberg, M., 2010. HPV vaccine suspension in India. Lancet 376 (9753), 1644–1645. Fernández, M.E., Allen, J.D., Mistry, R., Kahn, J.A., 2010. Integrating clinical, community, and policy perspectives on HPV vaccination. Annu. Rev. Public Health 31, 235. Glanz, K., Rimer, B.K., Viswanath, K., 2008. Health Behavior and Health Education: Theory, Research, and Practice. John Wiley & Sons. HPV vaccination [Internet], 2012. Available from: http://www.nhs.uk/conditions/hpvvaccination/pages/introduction.aspx?WT.mc_id=090805. HPV vaccine — questions &, answers [Internet], 2012. Available from: http://www. cdc.gov/vaccines/vpd-vac/hpv/vac-faqs.htm. Kaarthigeyan, K., 2012. Cervical cancer in India and HPV vaccination. Indian J. Med. Paediatr. Oncol. 33 (1), 7. Kohler, C.L., Grimley, D., Reynolds, K., 1999. Theoretical approaches guiding the development and implementation of health promotion programs. Handbook of Health Promotion and Disease PreventionKluwer Academic/Plenum Publishers, New York, NY pp. 23–49. Krupp, K., Marlow, L.A., Kielmann, K., et al., 2010. Factors associated with intention-torecommend human papillomavirus vaccination among physicians in Mysore, India. J. Adolesc. Health 46 (4), 379–384.

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Human papillomavirus vaccine acceptability among parents of adolescent girls: obstacles and challenges in Mysore, India.

Worldwide, 530,000 women are diagnosed with cervical cancer and 275,000 die annually. India bears the greatest burden of the disease with 132,000 case...
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