Acceptance patterns and decision-making for human papillomavirus vaccination among parents in Vietnam: an in-depth qualitative study post-vaccination

The burden of mortality from cervical cancer falls disproportionately upon women living in the developing world, where 88% of deaths from cervical cancer occur [1]. Cervical cancer is the second most common form of cancer among women in the developing world and the leading cause of cancer mortality for women. While cancer mortality has declined in high-income countries with improved screening and treatment services, the incidence of cervical cancer is projected to increase in middle- and low- income countries as their populations grow and age. By 2030, these countries will be home to an estimated 98% of cervical cancer deaths [1].

In light of the difficulty and cost of introducing effective and widespread screening services in low-resource settings, successful production of cervical cancer vaccines constitutes an important advancement for women's health. Currently, there are two vaccines—Merck’s Gardasil® and GlaxoSmithKline’s Cervarix®—that are highly effective in protecting against the strains of human papillomavirus (HPV) that cause 70% of cervical cancers. These vaccines have been licensed in more than 100 countries and, by the close of 2010, introduced in 33 national health programs. Though most of these national programs are in high-income countries, 20 developing countries have undertaken pilot projects to test the feasibility of introducing HPV vaccine on a national scale [2]. One such country, Vietnam, began testing strategies for HPV vaccine delivery in 2008, collecting data on coverage, acceptability, feasibility, and costs associated with integrating HPV vaccine into their National Expanded Program on Immunization (NEPI).

In low-resource settings, many factors influence the decision of whether and how to integrate a new vaccine into a national health program. Policymakers are increasingly asking for evidence of the impact a new vaccine is likely to have on communities as well as on the health care delivery system [3–5]. Based on research conducted in Latin America, Winkler et al. identified five distinct factors that shape the decision to introduce cervical cancer vaccines into public sector health programs: knowledge of cervical cancer incidence and its connection to HPV; affordability considerations; political will in the context of competing interests; the feasibility of vaccine delivery; and vaccine acceptability in the community [6]. It is this last decision-making factor—acceptability—that is the focus of this paper. As part of their decision-making process, policymakers want to know whether the vaccine will be accepted by those communities that will benefit, whether local opinion leaders will be supportive of a new vaccine, and whether support has been garnered among health providers who are asked to promote and deliver the new vaccine [7, 8].

In a recent literature review of studies exploring factors affecting HPV vaccine acceptance among adult women considering vaccination for themselves, Black et al. observed that the extent of knowledge of HPV infection and its connection to cervical cancer, the perception of risk for HPV infection or cervical cancer, the cost of the vaccine, and misinformation about HPV vaccine were all factors associated with vaccine acceptability for adult women [9]. Although the individual studies differ in methodology and focus, the main conclusion was that women generally were receptive toward HPV vaccine. An important caveat is that this review focused on studies of HPV vaccine acceptance in industrialized settings.

Far fewer studies address acceptability in developing country settings, prompting a call for further research [10]. A systematic review of HPV acceptability in nine countries in Asia Pacific included studies from India, Malaysia, Vietnam, Taiwan, Thailand, and South Korea (as well as Australia, New Zealand, and China) [11]. Despite the wide variation in methodology and approach, acceptability factors that emerged across a multitude of studies include perceived susceptibility to HPV (eight studies), perceived safety and side effects of the vaccine (twelve studies), concerns over effects on fertility (three studies), efficacy of the vaccine (six studies), and HPV vaccine recommendation by physician or social referent (seven studies). Research from Uganda presented similar areas of concern from parents [12], suggesting that motivating factors for parents related to HPV vaccine acceptance may be more universal than previously thought.

However, previous studies, including the reviews cited above, focus on “intent to vaccinate” prior to HPV vaccine availability or introduction. In Vietnam, we had the opportunity to examine parents’ rationales for either having or not having their daughters vaccinated and their decision-making process in the context of an on-going HPV vaccination demonstration project. This project, implemented by the National Institute for Hygiene and Epidemiology (NIHE), was designed to identify appropriate strategies for HPV vaccine delivery that could be integrated into NEPI. It targeted girls in grade 6 or 11 years old in four districts of two provinces, spanning urban, rural, and mountainous areas. The districts were selected based on cervical cancer disease burden, population size, geography, socioeconomic status, EPI performance, and staff capacities.

Most research on vaccine acceptability utilized a single type of measurement in exploring vaccine acceptability, often either a yes/no question [13, 14] or multiple items with a Likert scale [15–18]. Measures derived solely from quantitative survey data may not be sufficient for understanding the many facets of acceptability [19] and these types of measures are best employed in tandem with qualitative approaches. In this article, we present findings from qualitative research on parental reasons for HPV vaccine acceptance/non-acceptance and their decision-making process after both the first and second year of HPV vaccine implementation in Vietnam, and contextualize these qualitative data with recently published quantitative data on vaccine acceptability from this same project [20].

We designed a descriptive qualitative study of HPV vaccine acceptability among parents of girls eligible for vaccination in four districts of two provinces in Vietnam.^a Eligible girls for HPV vaccination were either 11 years of age (for the health-center based delivery strategy) or in grade 6 of primary school (for the school-based delivery strategy), of which more than 80% were 11 years of age, approximately 13% were 10 years old, and the remaining were 12 years old [20]. The study was implemented after the first year of vaccinations ended in June 2009 and repeated after the second year of vaccinations was completed in April 2010.

We used focus group discussions (FGD) and semi-structured interviews (SSI) to explore reasons for HPV vaccine acceptance or non-acceptance as well as to ascertain the process by which parents make their decision. FGDs were conducted with parents of fully vaccinated girls. Due to the very small number of girls who were partially vaccinated and the concentration of non-vaccinated girls in one urban location where school-based delivery was implemented,^b SSIs were conducted with parents of non- or partially-vaccinated girls. Additionally, in the Vietnamese context, not participating in a community-based vaccination program may have resulted in feelings of stigmatization among parents, inhibiting discussion of the reasons for their decision in a group setting. Individual interviews with these parents provide a more neutral, non-threatening environment to explore their decision. The key areas of inquiry included in the FGD guide and the SSI questionnaire were the same for both groups of parents. Key themes to elicit information about vaccine acceptability and the decision-making process were explored through a series of open-ended questions; some examples are provided below.

Questions for FGDs:

· What factors (personal, family, community, information, communication strategy) or individuals influenced your decision to have your daughter vaccinated?

· Please tell me how you made the decision about your daughter’s vaccination. Who raised the issue of HPV vaccination first, then who said what, and, who gave the final decision? Who, if anyone, did you discuss this with?

· Did anyone help you decide on whether to have your daughter vaccinated? Who influenced, why, how, and when?

Questions for SSIs:

· Why did your daughter not receive the full three doses?

· Were there any concerns that you had that kept you from taking your daughter (back) for vaccination?

· Please tell me how you made the decision about your daughter’s vaccination. Who raised the issue of HPV vaccination first, then who said what, and, who gave the final decision? Who, if anyone, did you discuss this with?

· Did anyone help you decide on whether to have your daughter vaccinated? Who influenced, why, how, and when?

Sampling process

The sampling process for study areas and populations varied from the first and second years of our study. As no study had yet been done of HPV vaccine acceptability after implementation of a HPV vaccination program, we selected a wide range of areas and large number of participants for our study after the first year of vaccinations. We performed criteria-based sampling for study areas using HPV vaccine delivery strategy implemented, type of geography (urban, rural, mountainous), and estimates of HPV vaccine uptake from NEPI reports. We used communes, administrative boundaries for health and other services in Vietnam, as the demarcation for study areas. All 72 communes that participated in the first year of the HPV vaccination program were classified by delivery strategy, type of geography, and low- or high-uptake based on NEPI reports (Figure 1). In each “geography-strategy” stratum, the three communes having the lowest uptake and the three with the highest were included in the sampling frame. From each group of three, one was randomly selected. The final sampling frame included 12 communes: ten communes had one FGD with parents of girls who received all three doses of HPV vaccine (fully vaccinated); and two communes with low uptake had SSIs with parents of girls who either were not vaccinated or received less than three doses (partially vaccinated). The rationale for sampling in this fashion was to ensure the inclusion of a range of different types of communes to reflect the geographic diversity of the country and the infrastructure capacities of communes that delivered HPV vaccines.

The sampling process after the second year of vaccinations was different, as nearly all 72 communes had achieved high uptake during the second year of program implementation and there was a purposive attempt to oversample communes where vaccine uptake was the lowest. Again using communes as the area of study and stratifying by delivery strategy, in mountainous areas, we used geographic access as a selection criteria for identifying one ‘easy to reach’ commune (less than ten kilometers from district center) from the school-based delivery strategy and one ‘hard to reach’ commune (more than 40 kilometers from district center) from the health center-based delivery strategy out of a total of 18 communes. In rural areas, we randomly selected two communes (from a total of 33 communes), one from each delivery strategy, from a list of seven that did not report 100% HPV vaccination uptake at dose two. In urban areas, two communes (from a total of 21 communes), one from each delivery strategy, were purposively selected based on the highest reported number of girls not vaccinated at dose two (Figure 2). An additional commune with the lowest vaccine uptake during the first year of implementation from the school-based delivery strategy was added to the sampling frame for parents of partially/non-vaccinated girls to investigate changes in this area over time (not included in Figure 2). The final sampling frame included seven communes, six of which had one FGD each with parents of fully vaccinated girls and the seventh had parents of partially/non-vaccinated girls who were selected for a SSI. This sampling strategy allowed us to focus in on any regional differences, as well as to highlight reasons for non-acceptance of HPV vaccination.

In Vietnam, the EPI system has a long history of development and has met with considerable success in reducing the burden of vaccine-preventable diseases. Its strong reputation contributes to a positive attitude in the population toward vaccination in general. The Vietnam HPV vaccine experience suggests that NEPI has succeeded in building trust by demonstrating the effectiveness of vaccination for disease prevention. We found evidence of this in expressions of belief in vaccination in principle, and the identification of government involvement as a rationale for accepting vaccination. Indeed, formative research prior to the vaccine demonstration project found that Vietnamese parents, teachers, health providers, and civic leaders voiced high levels of confidence in the government immunization program [5, 19]. For the general population in Vietnam, governmental programs are associated with high quality standards and rigor, so they are more likely to participate in these governmental programs rather than in seeking the same service from health providers in the private sector. The delivery of HPV vaccine by commune health center personnel and the additional involvement of local authorities brought credibility to the program and was a demonstration that the program was supported by the government.

While health rationales were preeminent, 12% and 20% of survey respondents in year 1 and 29% and 32% in year 2 indicated that the program being run by the government was a motivating factor. This survey response pattern was particularly evident in the mountain and rural regions, where parents were significantly more likely to say they were influenced by the fact that it is a government program (p<.000; data not shown). These findings echo what we observed in the FGDs in the mountain region, where government involvement in the program was a strong motivating factor.

While the cost of HPV vaccination was not the most common motivation, it emerged as a theme in the FGDs with parents of fully-vaccinated girls, particularly among participants from rural areas. However, formative research in Vietnam found that even for non donated vaccine, acceptance is still high as long as the price is affordable [5]. Moreover, analysis of year 2 survey data by region found no geographic differences in the identification of cost factors as a rationale for vaccine acceptance, calling into question whether economic considerations are more prevalent in some parts of the country than others [20].

Concerns about safety and vaccine side effects are a common refrain in HPV vaccine acceptability literature [11, 26–28] but suspicion about the vaccine and the intentions of HPV program planners (reflected in parents’ concern that children may be part of a vaccine trial) emerged less often. In part, this reflects the preponderance of studies from industrialized settings with strong regulatory systems in place (e.g., US, UK, Australia, and Canada). Indeed, a number of studies from developing countries have reflected concern that HPV vaccines are not well-tested (South Korea), concern over whom the vaccine has been tested on (Ghana), and suspicion over the involvement of foreign entities (India) [29–31]. Collectively, these findings suggest that addressing suspicions related to foreign involvement and the difference between demonstration projects (or scale-up) and vaccine clinical trials may be crucial considerations for HPV program planning in developing country settings. The need to involve influential government stakeholders in a visible fashion is another lesson learned from PATH’s experience in Vietnam, and elsewhere [32].

While concerns about vaccine impacts on fertility were cited by less than 10% of parents of non-vaccinated girls, the findings from Vietnam echo those from other studies of HPV vaccine acceptability in developing country settings [33]. More than one third of Chinese parents (38%) cited age as a rationale for not vaccinating [34] and more than two thirds of Ghanaian respondents (68%) expressed concerns about HPV vaccine impacts on fertility [30]. Our qualitative findings suggest that worry over the vaccine undermining a girl’s ‘natural development’ and compromising her immature health status may be connected to concerns about compromising her future fertility. These findings suggest that formative research to explore cultural perceptions of adolescent health and development and how conceptions of adolescence as a vulnerable period may impact HPV vaccine uptake could be beneficial in advance of vaccine introduction. They also speak to the need for information, education, and communication efforts that target any perception that young female adolescents are especially vulnerable to negative health effects from vaccination, wherever such perceptions are identified.

With respect to the decision-making process, we identified many active decision-makers—parents who sought out additional information to inform and confirm their vaccination decisions. Indeed, findings from a quantitative study of vaccine acceptability showed that more than four out of five parents reported that they had discussed HPV vaccination with someone prior to their decision in the first year. As the vaccination campaign matured in the second year (and coverage rates reached 97%), there was still more communication and discussion about the program. In this study, 94% of surveyed respondents in Year 2 reported that they had discussed HPV vaccination with someone prior to making a decision [20]. Moreover, active decision-makers were significantly more likely to accept vaccination than passive decision-makers who made a decision without discussion (data not shown).

The high prevalence of active decision-making in Vietnam is quite consistent with results from the UK, where only 14% of parents based their HPV vaccine decision solely on information provided by the program [35]. However, that study identified a very intransigent population of active refusers, who, the authors felt, would be unlikely to change their minds despite exposure to additional information [35]. While these findings may suffer from selectivity bias, if active refusers are more likely to respond to the survey and attend information nights, the findings raise intriguing questions about the ability of vaccine campaigns to change entrenched anti-vaccine attitudes.

The existence of ‘active refuser’ populations who believe that vaccination may have negative, long-term, and unknown side effects is a widespread phenomenon. In the Netherlands, resistance to polio vaccination was sometimes based on religious conviction [36]. Highly educated parents may resist MMR vaccine on the belief that it ‘impairs the immune system’ [37]. Similar ‘anti-vaccination’ attitudes have been observed among parents with respect to HPV vaccine in Australia [38]. Indeed, anti-vaccination attitudes were common enough among parents in Australia that Cooper Robbins and colleagues, employing a conceptual framework similar in many respects to the model we use, identify ‘anti-vaccination’ as a separate decision-making state, distinct from active and passive decision-making. Our qualitative findings, in the context of a very high rate of vaccine uptake, particularly in the second year (97%) and among active decision-makers, suggest that such entrenched anti-vaccine (or anti-HPV vaccine) attitudes are yet to take root in Vietnam.

Our findings about the importance of active decision-making in a developing country setting generate several implications. First, to maximize effectiveness, communication campaigns may need to employ a broad brushstroke, targeting influential figures, teachers, health workers, and other members of the public; regardless of any direct involvement in the program, these individuals may influence uptake indirectly, through informal consultations. The second concerns the possibility that discussion with others may quell vaccine-related concerns and/or generate the perception of broader community support for vaccination. Researchers may want to explore further if and how dialogue facilitates decision-making and contributes to vaccine uptake. Third, program planners would do well to anticipate the need for active decision-making in the scheduling of vaccination campaign activities by providing information well in advance of the scheduled vaccination drive.

Parents in Vietnam were motivated to allow their daughters to receive HPV vaccine by health rationales and by the involvement of the government (NEPI) in the vaccine program. Those who declined participation were influenced by concerns for vaccine safety and side effects, suspicions related to the newness and possible experimental nature of the vaccine, and concerns about negative health impacts of vaccinating adolescent girls. Like parents in high-resource settings, Vietnamese parents are active decision-makers, frequently seeking out additional sources of information to inform and confirm their vaccination decisions. Vietnam’s HPV vaccination experience speaks to the importance of close collaboration with the government to make the most of existing high levels of trust, and to reduce suspicions about new vaccines that are a natural component of vaccine demonstration projects. Cervical cancer continues to be a leading cause of death for women throughout the developing world. Experiences in Vietnam should be shared in a wider context to reduce the lag time between when a new vaccine becomes available in the market and when it is incorporated into national health programs in low-resource countries.

^aA separate study assessed vaccine acceptability among girls who were eligible for HPV vaccine. Results are presented in the following document: PATH and Vietnam National Institute of Hygiene and Epidemiology. Evaluating HPV Vaccine Delivery Strategies in Vietnam. Seattle, Washington: PATH; 2010.

^bOf the 508 total eligible girls either not vaccinated or partially vaccinated, only 27 (5.3%) were partially vaccinated, which represents 0.8% of all girls who received the first dose of vaccine. Of the 481 total eligible girls not vaccinated in the first year, 73% resided in one urban area that implemented school-based delivery.

^cThe sex of the parent was collected only for FGD participants, so precise distribution of mothers and fathers is not available.

^dWe occasionally cite previously published findings from a representative survey of parents whose daughters were eligible for HPV vaccine during a demonstration project in Vietnam. A full description of this survey’s methodology has been previously published (LaMontagne DS et al., 2011).

^eThe data in Table 2 represents the range across the two delivery strategies (school-based and health center-based) and program years.

^fNote that we replicate here only data published on the first year of the project, given very high coverage rates and only 14 surveyed parents with a partially- or non-vaccinated child in the second year.