Knowledge of Cervical Cancer and HPV Vaccine Post-Vaccination among Mothers and Daughters in Vietnam

Cervical cancer is one of the leading causes of cancer related mortality in women (Ferlay et al., 2010). Availability of human papillomavirus (HPV) vaccine offers a method of primary prevention and has the potential to significantly reduce cervical cancer incidence and deaths (Brotherton et al., 2011). Prior to initiating an HPV vaccination program, assessing the levels of knowledge and awareness in a community has been suggested as a means to develop appropriate educational materials for vaccine recipients and decision-makers (Bingham et al., 2009; Jacob et al., 2010). A number of studies in Vietnam and other Asian countries have reported low levels of knowledge about cervical cancer, HPV, and HPV vaccines (Loi & Nhung, 2004; Dinh et al., 2007; Nghi et al., 2010; Young et al., 2010; Charakorn et al., 2011). These and other HPV vaccine acceptability studies have assessed knowledge and vaccine intentions before HPV vaccine availability (Allen et al., 2010). Although some studies have reported little or no relationship between HPV knowledge and vaccine acceptance, there is a belief


Introduction
Cervical cancer is one of the leading causes of cancer related mortality in women (Ferlay et al., 2010).Availability of human papillomavirus (HPV) vaccine offers a method of primary prevention and has the potential to significantly reduce cervical cancer incidence and deaths (Brotherton et al., 2011).Prior to initiating an HPV vaccination program, assessing the levels of knowledge and awareness in a community has been suggested as a means to develop appropriate educational materials for vaccine recipients and decision-makers (Bingham et al., 2009;Jacob et al., 2010).A number of studies in Vietnam and other Asian countries have reported low levels of knowledge about cervical cancer, HPV, and HPV vaccines (Loi & Nhung, 2004;Dinh et al., 2007;Nghi et al., 2010;Young et al., 2010;Charakorn et al., 2011).These and other HPV vaccine acceptability studies have assessed knowledge and vaccine intentions before HPV vaccine availability (Allen et al., 2010).Although some studies have reported little or no relationship between HPV knowledge and vaccine acceptance, there is a belief

Knowledge of Cervical Cancer and HPV Vaccine Post-Vaccination among Mothers and Daughters in Vietnam
Proma Paul1 , D Scott LaMontagne2 *, Nga Thi Le 2 that limited knowledge may be a barrier to HPV vaccine acceptance (Sarin 2008;Charakorn et al., 2011).
A two-year demonstration project of HPV vaccine delivery was recently completed in Vietnam, achieving high coverage in both school-and health center-based approaches (LaMontagne et al., 2011).Parents reported that prevention of cervical cancer was a primary reason for accepting the vaccine (LaMontagne et al., 2011).However, their specific knowledge of cervical cancer or HPV vaccine as a prevention method has not yet been reported.As part of the demonstration project in Vietnam, awareness campaigns and education sessions about cervical cancer and HPV vaccines, based on results of previous formative research on these topics (Nghi et al., 2010), targeting vaccine-eligible girls, parents, and the broader community were designed and implemented prior to initiation of vaccinations.Key messages and communication strategies for the community centered around the burden of cervical cancer in Vietnam, the use of vaccines as a method of prevention, and the safety and potential side-effects of HPV vaccines (Nghi et al., 2010).
The object of this study was to assess knowledge of cervical cancer, HPV infection, and HPV vaccines among parents and girls exposed to an education campaign as part of the HPV vaccine demonstration project conducted in Vietnam, to compare the knowledge of these areas between mothers and daughters, and to explore whether knowledge was associated with vaccination status.

Materials and Methods
Two rounds of operational research were conducted; one after each year of HPV vaccine delivery was completed.This research used a mixed-methods approach to assess vaccine coverage achieved by the delivery strategies (LaMontagne et al., 2011), acceptability of HPV vaccine, feasibility of the vaccination program (PATH & NIHE, 2011), and the costs of delivery (Levin et al., 2011).During the first round of operational research, adjunct knowledge, attitudes, and practice (KAP) questions were asked in conjunction with the survey used to measure vaccine coverage.

Study design
An adaptation of the World Health Organization immunization coverage cluster survey was used to assess HPV vaccine coverage and reasons for vaccination (WHO, 2005).The detailed description of the study's methodology has been previously reported (LaMontagne et al., 2011).In short, a two-stage cluster sampling method was used to select households with vaccine eligible girls.At eligible households, parents/guardians were invited to participate in the coverage survey and respond to supplemental KAP questions.Respondents were primarily mothers.Girls who were eligible for HPV vaccine were also invited to answer the supplemental KAP questions.We limited our analysis to households where both a mother and her daughter responded to the KAP questions in paired mother-daughter interviews.
Data collected through the KAP questions included knowledge of cervical cancer, HPV, and the HPV vaccination program; attitudes towards HPV vaccination and the HPV vaccination program; and practices related to exposure to and satisfaction with information, education, and communication (IEC) materials and health education messages.Questions exploring different aspects of knowledge were developed based on the information included in the educational materials that parents and girls were given prior to vaccinations.

Data collection and analysis
Data were collected using a structured questionnaire that was developed in English and then translated into and administered in Vietnamese.Questions asked of girls were tailored to a grade 6 level.Surveys were administered separately: the mother first, followed by the daughter.Coded responses were recorded on a data recording sheet.Descriptive statistics were used to characterize the study population.
A scaled composite knowledge measure was created for the following knowledge parameters: cervical cancer, HPV, and HPV vaccine with point values of five, two, and three respectively, corresponding to one point for each question covered in each knowledge parameter.If a question had multiple correct answers, the question was assigned one point for at least one correct answer.The participant's maximum knowledge score was ten.Mean scores of overall knowledge and specific knowledge parameters were calculated for mothers and daughters.Differences in mean knowledge scores between mothers and daughters and between fully vaccinated and partially/ non-vaccinated populations were measured by t-test, with statistical significance of p <0.05.Data were analyzed using Stata 10.0 (StataCorp, 2009).

Ethical considerations
Parents/guardians interviewed gave verbal consent prior to survey administration.At the time of this interview, parents/guardians were also asked to provide verbal permission to administer the supplemental KAP questions to their daughter.Girls were also requested to assent verbally to participate.If the parent/guardian did not allow their daughter to participate or the parent/guardian granted permission but the girl dissented, only the parent/ guardian was interviewed.
This study received ethical approval from institutional review boards in the United States (PATH, Seattle, USA) and Vietnam (Vietnam Ministry of Health, Hanoi, Vietnam).

Characteristics of survey participants
Among the 780 parent/guardians who completed the coverage survey and KAP questions, 757 had corresponding KAP responses from an eligible girl, with 536 (70%) mother-daughter paired interviews.Most of the households interviewed were in urban areas (57.8%); less than 4% of the mothers had no formal education and the majority of the daughters (82.1%) were 11 years old (Table 1).Eighty-seven percent of the girls interviewed had received all three doses of the HPV vaccine.

Perception of information received
When asked whether enough information was received, 73.3% and 78.2% of mothers and daughters, respectively, reported receiving enough information about cervical cancer.Approximately two-thirds of mothers and three-quarters of daughters reported that they received enough information about the HPV vaccine.The large majority of mothers and daughters felt the information received was sufficient to make a decision about vaccine acceptance (90.1% and 88.3% for mothers and daughters, respectively) (Table 1).

Cervical cancer and HPV vaccine knowledge
Out of the 1,072 mothers and daughters interviewed, nearly 40% of respondents did not know that cervical cancer was the most common cancer from which Vietnamese women die, nor did they know how to prevent cervical cancer.Less than 50% of mothers and 20% of daughters knew the peak age of cervical cancer (Table 2).
One hundred and sixty-two respondents, 119 mothers and 43 daughters, identifying at least one symptom of cervical cancer, reported the most common symptom identified was pain in the pelvic area (55.6%), followed by breakthrough bleeding (29.6%), and irregular discharge (21.6%).Among the 235 respondents (150 mothers and 85 daughters) who correctly identified at least one cervical cancer risk factor, the most common risk factor reported was early initiation of first sexual experience (65.1%).Approximately 50% of mothers and daughters knew that HPV causes cervical cancer, but 28.9% and 19.9% of mothers and daughters, respectively, knew how HPV is transmitted.Although more than 80% of mothers and daughters knew the purpose of the vaccine, 201 (37.6%) mothers and 133 (24.8%) daughters did not know the eligible population for HPV vaccines (Table 2).

Comparison of knowledge between mothers and daughters
Based on the mean knowledge scores for each of the parameters, mothers and daughters recalled different information during the survey (Table 2).Generally, mothers had more knowledge about cervical cancer and HPV infection compared to daughters (p<0.01).Daughters had more HPV vaccine specific knowledge (p<0.01).However, the overall mean knowledge score was similar for the two groups, 5.0 (standard deviation 2.1) for mothers and 5.0 (standard deviation 1.8) for daughters (p=0.74).Modest positive correlation between mothers' overall knowledge scores and their respective daughters was observed, r=0.356,N=536, p<0.001, demonstrating similar level of knowledge about cervical cancer and HPV vaccines between mothers and their daughters.

Comparison of and HPV vaccination status
Fully vaccinated girls had a 1.7 points higher mean knowledge score compared to partially or non-vaccinated girls (p<0.01)(Table 3).The trend was similar among mothers of vaccinated partially or non-vaccinated girls.The mean knowledge score for mothers of fully vaccinated girls was 5.3 (standard deviation 2.0) and the mean knowledge score for mothers of partially or non-vaccinated girls was 3.4 (standard deviation 2.4) (p<0.01).
For mothers, correctly answering questions about peak age of cervical cancer (p=0.49),cervical cancer risk factors (p=0.17), and HPV transmission (p=0.59) were not statistically significant by vaccination status.Daughter's knowledge about symptoms of advanced cervical cancer (p=0.08) and peak age of cervical cancer (p=0.17) were not different among fully and partially/non-vaccinated girls.However, information about the magnitude of the cervical cancer problem in Vietnam (p<0.01),being aware that HPV causes cervical cancer (p<0.01), and general HPV vaccine information, such as purpose of vaccine, target recipient, and potential side-effects (p<0.01), were significantly different by vaccination status for both mothers and daughters (Table 3).

Discussion
Prior to HPV vaccine delivery in the demonstration sites in Vietnam, formative research in these areas (Nghi et al., 2010), as well as previous studies in Vietnam and other Asian countries, reported the limited knowledge about cervical cancer and low to no knowledge about HPV vaccines (Loi & Nhung, 2004;Dinh et al., 2007; Young et al., 2010;Charakorn et al., 2011).Our study investigated knowledge levels of daughters and their mothers who were exposed to HPV vaccine messaging as part of the communication strategy of a vaccination program, exploring the relationship between knowledge of mothers and their respective daughters.The total mean knowledge score, approximately five out of ten, was similar for mothers and daughters in the survey population, indicating that only half of the knowledge questions were answered correctly.These findings show that both mothers and daughters have low levels of knowledge about cervical cancer, HPV infection, and HPV vaccines even after an intensive education campaign primarily conducted immediately prior to the first HPV vaccine dose.
Notably, our findings suggest that knowledge about certain topics may have improved after the education and communication campaigns.In formative research conducted prior to the implementation of HPV vaccinations in these communities in Vietnam, researchers noted a general lack of knowledge and awareness about the existence of HPV vaccine and its use to prevent cervical cancer (Nghi et al., 2010).However, our survey found most mothers and daughters had heard of HPV vaccine and knew what it could prevent.These results suggest that the message about the purpose of the vaccine was clearly disseminated and understood by mothers and daughters, and specifics about the HPV vaccine were understood by the recipients of the vaccine.
Even though the communication content was similar for parents and girls, our results indicate that mothers and daughters may have received different information, or retained/recalled different information of relevance to them: mothers' recalled information focused on cervical cancer and daughters' recalled information focused on the vaccine.This difference may be due to presentation and relevance of the information being presented (Kreuter & Wray, 2003;Wilson, 2007).Mothers' knowledge about cervical cancer may be linked to their perceived risk about developing cervical cancer.Similarly, the vaccine related knowledge that daughters had may be due to the fact that they were receiving the vaccination.
Although knowledge was low, eligible girls in this population were highly likely to receive all three doses of HPV vaccine (LaMontagne et al., 2011), suggesting that specific HPV and cervical cancer knowledge may not be a primary driver for HPV vaccine acceptance, a finding similar to that recently reported from the Australian HPV vaccination program (Cooper et al., 2010).Previous findings from childhood immunization programs have suggested that specific knowledge about immunizations and the diseases they protect against are not necessarily associated with vaccine acceptance (Nichter, 1995;Jhetta & Newell, 2008).It is also important to note that both mothers and daughters reported receiving sufficient information about cervical cancer and HPV vaccine to make a decision about accepting HPV vaccine.Therefore, education campaigns for new vaccines should be clear on what information they want to communicate to communities balanced with what information families need to make a decision for vaccine acceptance, recognizing that the information may not necessarily be the same for both.
Nevertheless, the higher mean knowledge of fully vaccinated girls and their parents, when compared to partially/non-vaccinated girls and their parents suggests that limited knowledge about magnitude of cervical cancer, HPV as the cause of cervical cancer, and general information about HPV vaccinations may have contributed to incomplete vaccination.Therefore, communication and education campaigns may want to focus on these messages to facilitate vaccine uptake.Given the correlation between daughters' overall knowledge and their mothers' overall knowledge, comprehensive cervical cancer messaging that covers both vaccination and screening may help reinforce messages to both groups.
Our study has a few limitations that should be kept in mind when interpreting our results.First, respondents in our study were asked cervical cancer and HPV vaccine knowledge questions nine months after the initial education campaigns.Recall of information may have been different if respondents were asked the same set of questions immediately after the campaign, such as after the administration of the first dose.The study was unable to assess whether respondents knew the information and forgot it, never knew it, or if it was related to how many times they were exposed to the key message.Lastly, due to the cross-sectional nature of the study, as well as the small number of daughters not vaccinated, we cannot conclude that the information disseminated determined vaccine acceptance, as that decision could have also been influenced by other factors, such as fear of cancer, wishes of the father, familial history, or experience with cervical cancer, amongst others.Even given these limitations, our study still provides valuable insight into knowledge retention and recall with a population-based sample of mothers and daughters, a particular strength in our design.
In conclusion, the results from this study suggest knowledge of daughters and their mothers alone may not be the deciding factor for HPV vaccination, since vaccination uptake was high even with low overall knowledge.Even if comprehensive information on cervical cancer, HPV vaccines, and the program is provided to the communities, mothers and daughters may also remember different aspects of an HPV vaccine education campaign.Individuals may rely on certain pieces of information that they feel are more important to them.Since mothers of girls who did not complete the vaccination series or who were not vaccinated at all seem to have limited knowledge about cervical cancer, HPV as its cause, and HPV vaccines more generally, future education campaigns may want to ensure that these key messages are included.Further research is needed to assess and understand the precise requirements of a communication strategy for HPV vaccines that results in high uptake: what pieces of information, to which audiences, how often, and to what degree of saturation.
by Merck & Co., USA.Neither the funder nor vaccine manufacturer was involved in the study design and implementation, data collection and analysis, or writing of this manuscript.We also thank national, provincial, regional, district, and commune immunization and education programmes and their staff for their support during the HPV vaccine demonstration project and the operations research conducted thereafter.We acknowledge the leadership of national and provincial partners in this project, including the National Institute of Hygiene and Epidemiology, National Center for Health Education and Communication (CHEC), provincial CHECs, Consultation of Investment in Health Promotion (CIHP), the Thanh Hoa Reproductive Health Center, and the Medical Colleges of Can Tho and Thanh Hoa.We extend thanks to Nguyen Quy Nghi, Trinh Thu Huong, Tran Hung Minh, and Bui Thi Thanh Mai who were a part of the original study team and conducted the field data collection; Allison Bingham, YiJia Tang, and Amynah Janmohamed for initial reviews of this study; and Vivien Tsu for critical review of the final manuscript.We also express our gratitude to mothers and daughters for their time and participating in this study.