https://doi.org/10.1177/17455057231172355 Women’s Health
Volume 19: 1 –12
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Knowledge and attitudes of mothers
toward HPV vaccination: A cross-sectional study in Kazakhstan
Aisha Babi
1* , Torgyn Issa
1* , Alpamys Issanov
2, Sholpan Akhanova
3, Natalya Udalova
4, Svetlana Koktova
5, Askhat Balykov
5,
Zhanna Sattarkyzy
6, Balkenzhe Imankulova
7, Nazira Kamzayeva
7, Wassim Y. Almawi
1,8and Gulzhanat Aimagambetova
9Abstract
Background: Although recommended for all member states of World Health Organization, there is no national human papillomavirus vaccination program in Kazakhstan. Furthermore, there are no studies in Kazakhstan that evaluate the mothers’ perception of human papillomavirus vaccines.
Objectives: This study aims to assess the knowledge and attitudes toward human papillomavirus vaccination among mothers in Kazakhstan and the factors associated with their attitudes.
Design: A cross-sectional study was performed during the period of December 2021—February 2022. The STROBE guideline for cross-sectional studies was applied.
Methods: Paper-based structured questionnaires were filled out by 191 mothers, 141 of whom had daughters. The attitude score was assessed as per the Likert-type scale. The Chi-square and Fisher’s exact tests, with a significance value of < 0.05 were used to analyze the relationships between the characteristics of mothers and their attitude scores.
Results: The following factors were significantly associated with mothers’ attitudes toward human papillomavirus vaccination: a place of residence, family income, number of children, and refusal of vaccination for themselves (p < 0.005).
Of all participants, only 45% of all mothers, 41% of mothers with a female, and 46% of mothers with male children had positive attitudes toward human papillomavirus vaccination. The child’s gender was not a significant determinant.
Overall, the level of knowledge about human papillomavirus vaccination was found to be low. The median total score is 0 out of 12 for women who have negative and neutral attitudes toward human papillomavirus vaccines. Among women who have positive attitudes toward HPV vaccines, the median score is around 3 points.
Conclusion: Before the implementation of the human papillomavirus vaccination program into the Kazakhstani national vaccination calendar, comprehensive and adequate information and education campaigns are required on the national level for parents and the population in general.
Keywords
HPV vaccination, HPV vaccine attitude, HPV vaccines, Kazakhstan, mothers’ attitude
Date received: 28 September 2022; revised: 7 April 2023; accepted: 11 April 2023
1 Department of Biomedical Sciences, School of Medicine, Nazarbayev University, Astana, Kazakhstan
2 Department of Medicine, School of Medicine, Nazarbayev University, Astana, Kazakhstan
3 Obstetrics and Gynecology Department, “Keruen Medicus” Clinic, Almaty, Kazakhstan
4 Obstetrics and Gynecology Department, East-Kazakhstan Regional Hospital, Oskemen, Kazakhstan
5Regional Perinatal Center, Aktobe, Kazakhstan
6 Obstetrics and Gynecology Department, City polyclinic #6, Astana, Kazakhstan
7 Clinical Academic Department of Women’s Health, CF University Medical Center, Astana, Kazakhstan
8Faculty of Sciences, El-Manar University, Tunis, Tunisia
9 Department of Surgery, School of Medicine, Nazarbayev University, Astana, Kazakhstan
*These authors had equal contribution.
Corresponding author:
Gulzhanat Aimagambetova, Department of Surgery, School of Medicine, Nazarbayev University, Kabanbay batyr street, 53, Astana 010000, Kazakhstan.
Email: [email protected]
Original article
Introduction
Human papillomavirus (HPV) is a virus that infects the skin and mucosal cells.1 Of more than 200 known HPV genotypes, 14 high-risk types are associated with cervical cancer, anogenital cancers, and head and neck cancers.1 HPV-16 and HPV-18 types are responsible for up to 75%
of all cervical cancerases.2,3 Moreover, HPV is highly transmissible, and most people may become infected at some point in their lives, with the peak incidence of HPV occurring soon after the sexual debut.1
Limited data were available on HPV genotype- specific prevalence and the burden of cervical cancer in Kazakhstan.4 Earlier pilot studies reported the preva- lence of high-risk HPV in Western Kazakhstan5 and the capital city Astana.6 More recent regional studies on HPV prevalence among Kazakhstani women reported high-risk HPV infection in 39% of study participants,7,8 which in turn leads to a high incidence of cervical can- cer.9,10 In 2020, there were 1,777 cases of cervical cancer and 834 related deaths in Kazakhstan, with the crude incidence rate among females equal to 18.4 per 100,000 population.11
Three HPV vaccines are currently approved by the World Health Organization (WHO); all are protective against HPV-16 and HPV-18.12 HPV vaccination target groups are young adolescent girls and boys, aged between 9 and 14 years, and are efficient in preventing precancerous cervical lesions caused by high-risk HPV types.1 Moreover, the WHO Global Action Plan for the Prevention and Control of Non-communicable Diseases 2013–2020 identified HPV vaccination as the best buy and recommends including it in the national health plan.13 One of the three targets of the Global strategy to accelerate the elimination of cervical cancer as a public health problem is to fully vaccinate 90% of teenage girls under the age of 15 years.13
HPV vaccines are proven to be safe and their efficacy in preventing HPV-related conditions is well recog- nized.12,14,15 The effectiveness of the HPV vaccination was also demonstrated by the drastic reduction in cervi- cal cancer cases among vaccinated women in Scotland,16 Finland,17 Denmark,18 and the United States.19
Although recommended for all member states of WHO, HPV vaccination was not implemented in Kazakhstan yet.20,21 An attempt at HPV vaccine implementation was made in 2013; however, the program was shortly closed after negative media coverage and concerns raised by par- ents.22 This was similar to what was seen in Japan, where reports of vaccine side effects dampened the success of the program, reducing the coverage to less than 1%.23 Parental hesitancy toward the HPV vaccine is a major determinant of the vaccination program’s low coverage, as parental permission is a prerequisite for vaccine administration among children and adolescents in many countries, as liv- ing with a vaccine-hesitant parent lowers the likelihood of a teen receiving a vaccination by almost 70%.24–26
The responsibility for children’s health and well-being often falls on mothers rather than fathers or other rela- tives.27,28 In families where mothers were decision-mak- ers of children’s vaccination, the proportion of vaccinated children was significantly higher than in families with a decision-maker other than the mother.29 There is a high, almost blind, level of trust among teenage girls in their mother’s decision about HPV vaccines, most of whom followed the arguments of their mothers, despite the girls’
interviews conducted separately from the parent, further demonstrating the key role mothers play in their chil- dren’s vaccination.30
A major factor affecting parents’ attitudes toward HPV vaccines and intent to use it is the level of knowledge the parents have about the vaccine and their level of educa- tion.31,32 The politicization of information about HPV vaccines causes increased confusion and likely negative emotional response.33 On the other hand, providing rele- vant medical information increases acceptance of the HPV vaccine.34 It is important to establish the contri- bution of the lack of knowledge as a major determinant for inadequate HPV vaccine acceptance. This study aims to characterize mothers as to their attitudes toward HPV vaccination in Kazakhstan, investigate the correlation between HPV knowledge and attitudes toward HPV, and describe the main sources of HPV information for Kazakhstani mothers. In addition, this study aims to understand whether mothers who have daughters have a different HPV vaccine attitude than mothers of only boys.
Methods
Study design and population
A cross-sectional study was conducted between December 2021 and February 2022. The STROBE guideline for cross- sectional studies was followed. Paper-based questionnaires were collected in outpatient clinics of four large cities in Kazakhstan (Astana, Almaty, Aktobe, Oskemen). The fol- lowing inclusion criteria were applied for this research: (1) women of 18 years and older, (2) who have children, and (3) and able to understand Kazakh and Russian (two lan- guages officially used for communication in the Republic of Kazakhstan). Women younger than 18 years, those with- out children, and unable to communicate in one of the State languages were excluded. Thus, mothers aged 18 years and older were recruited to participate in the study (Appendix A, Study Protocol) by their gynecologist during the regular check-up on a voluntary basis, and no incentives for partici- pation were used. A convenient sampling technique was used for the study participants’ recruitment among women attending gynecological clinics for regular medical check- ups. After a careful explanation of the study’s aims, a total of 399 women were invited to take part in the survey. Out of 399 approached, 347 agreed to take part in the survey.
However, only 191 mothers filled out the study question- naire. The response rate was 55%.
Study instrument
The study instrument was a paper-based survey com- posed of two parts. The first part of the questionnaire assessed the social and demographic characteristics of mothers; the second part was adapted from the French Survey Questionnaire for the Determinants of HPV Vaccine Hesitancy (FSQD-HPVH) and consisted of 29 questions, which assessed mothers’ beliefs and attitudes toward HPV vaccination (Appendix B, Study Survey).35
The adapted questions were translated and back-trans- lated into Kazakh and Russian languages with the help of independent trilingual (English-Russian-Kazakh) inter- preters. The process of the translation/adaptation followed a recommended guideline for cross-cultural adaptation of self-report measures.36–38 and consisted of the following stages: forward translation, synthesis of the forward trans- lation, back translation, expert committee review, and testing of the version. Discrepancies in translations/inter- pretations were resolved after thorough discussions. The Kazakh and Russian translated versions of the second survey were piloted among 15 participants to assess the clarity and appropriateness of the translated items and responses. The survey was conducted in Kazakh and Russian depending on the participants’ preferences.
Study variables
Independent variables analyzed in the study were socio- demographic characteristics of mothers: age, ethnicity, the highest attained education, city, and marital status, number of children and their gender, and household income. The mothers were grouped by quartiles into four age groups:
20–29 years old, 30–36 years old, 37–45 years old, and 46 years old and older. Ethnicity was categorized into two groups: Kazakh and other ethnicities. The highest attained education was divided into three groups: high school or below, college, and university. Children’s number were categorized into two groups: 1–3 children, and 4 or more children, which is a social category recognized by Kazakhstan’s government and eligible for governmental benefits (https://adilet.zan.kz/rus/docs/V1500011507).
Furthermore, a child’s gender was described separately in two categories: mothers with sons only, and mothers with daughters or daughters and sons. In February 2022, the average income in Kazakhstan was 272 968 tenge (≈600USD).39 Accordingly, the household income was categorized into three groups: below average income (low), within average income (middle), and above average income (upper income).
Information about mothers’ medical history, including refusal of any vaccination, and history of abnormal Papanicolaou test (Pap-test) results was collected. For mothers who have daughters, there was additional infor- mation about mothers’ choices regarding their daughters’
health, including refusal of any vaccination for daughter,
difficulty talking to daughter about her sexual health (Disagree, Neutral, Agree), discomfort in discussing daughter’s sexual health with a doctor or other healthcare professional (Disagree, Neutral, Agree), difficulty bring- ing up the subject of the HPV vaccine to daughters (Disagree, Neutral, Agree).
The dependent variable was mothers’ attitudes toward HPV vaccination. The outcome variable was measured using 4 positive and 4 negative statements on the Likert- type scale. Mothers’ attitude was categorized as negative (mean score < 3), neutral (mean score 3), and positive (mean score > 3) to separate women who have not demon- strated neither positive nor negative disposition toward the vaccine. In addition, mothers who have daughters answered 4 more items to further study their attitude, with a total of 12 statements on the Likert-type scale.40,41 The attitude of mothers of daughters was categorized as nega- tive (mean score < 3), neutral (mean score 3), and positive (mean score > 3).
The knowledge of mothers about HPV and the HPV vaccine was assessed with 12 true/false questions. A cor- rect answer was given 1 point, and an incorrect or “I don’t know” answer was given 0 points. The participants were also asked if they ever searched for information about the HPV vaccine, which sources they used, and whether the information was useful in deciding about the vaccine.
Sample size calculation
The OpenEpi online application to calculate the required samples for dichotomous outcomes was used.42 Since there is insufficient data on knowledge and attitudes toward HPV vaccination among mothers in Kazakhstan, we assumed the proportion of knowledgeable mothers or mothers with positive attitudes was 50%. In calculating the sample size, the following parameters were applied—
alpha = 0.05, power = 0.80, and the anticipated proportion of knowledgeable mothers or mothers with positive atti- tudes at 50%. The suggested sample size was 384.
Ethical considerations
The study was conducted in compliance with the Decla- ration of Helsinki and was approved by the Institutional Research Ethics Committee (IREC) of Nazarbayev University on April 23, 2019 (IREC number: 146/4042019).
All study participants were informed about the aims, meth- ods, risks, and benefits of the study prior to participation in the study.
After the explanation of the voluntary and anonymous nature of the study, verbal consent was obtained from the study participants. The verbal consent was considered the most appropriate to fulfill the anonymous nature of the study. Moreover, the choice of verbal consent was dictated by the cultural context of Kazakhstan as a post-Soviet country, where people are not comfortable with “signing
documents that are similar to a contract.”20 Verbal consent used for this study included all the necessary components for informed consent (Appendix C, Verbal Consent). No personal information related to any of the participants was available to the research team. The statements on the study participants’ rights were declared orally and in the infor- mation letter provided to the participants.
Statistical analyses
Statistical analysis was performed using STATA 16.43 We performed descriptive statistics by presenting continuous data as means and standard deviations, and categorical data as absolute and relative frequencies. Chi-square or Fisher’s exact tests, where appropriate, with a significance value of < 0.05 were used to analyze relationships between categorical variables. Ordinal logistic regression was per- formed to explore factors associated with attitudes toward HPV vaccination among mothers. Variables that showed significance in the bivariable analysis and were important as epidemiological factors were included in the final model. The goodness of fit of the model was checked with Hosmer–Lemeshow, Pulkstenis–Robinson Chi-square, and deviance tests, as well as the Lipsitz likelihood-ratio test.
Results
Description of the study subjects
A total of 191 mothers agreed to participate in the study.
Table 1 shows the socio-demographic characteristics of the study participants, that is., mothers. The mean age of the participants was 37.3 ± 10.1 years. The mean age of having the first child was 24.2 ± 4.5 years. There was a comparable distribution of women in the four age groups, and equal distribution of participants from the different regions of Kazakhstan. Most mothers were of Kazakh eth- nicity (80%), had a university degree (54%), had a low level of family income (48%), and were in a committed relationship (84%). Of all participants, 85% had 1–3 chil- dren, and 74% had daughters. Less than half (39%) of mothers have confirmed refusing vaccination in principal for themselves in the past, with 16% of mothers having a history of abnormal Pap-test.
Table 1 also shows the characteristics of mothers who have daughters. The mean age of participants was 37.9 ± 10.3 years. The mean age of having the first child was 24.0 ± 4.5 years. The majority of mothers in this group had 1–3 children (81%), and 45% refused a vaccine for their daughters. The same proportion of respondents (45%) disagreed that it is hard to talk to their daughters about their sexual health, and having difficulty bringing up the subject of HPV vaccines with their daughters. Half of the mothers (50%) disagreed with being uncomfortable discussing their daughter’s sexual health with a doctor, or other healthcare professionals.
Attitudes toward HPV vaccination
Table 2 shows mothers’ attitudes toward HPV vaccination and participants’ characteristics. Among all mothers, only 45% had positive attitudes toward HPV vaccination.
Significantly associated characteristics were a place of residence, family income, number of children, and refusal of vaccination for themselves (p < 0.005). Irrespective of their residence, the majority of mothers had positive atti- tudes toward HPV vaccination. Except for Aktobe, where most participants had neutral attitudes toward HPV vacci- nation. Irrespective of family income, most mothers had positive attitudes toward HPV vaccination, and half of the mothers (51%) had positive attitudes toward HPV vacci- nation. In the case of mothers with 4 or more children, more than half (57%) had neutral attitudes toward HPV vaccination. Among mothers who did not refuse vaccina- tion for themselves, half (51%) had positive attitudes toward HPV vaccination. However, among mothers who refused vaccination, there was a comparable distribution of three levels of attitudes toward HPV vaccination.
Among mothers of daughters, 41% had positive attitudes toward HPV vaccination (Table 2). Statistically significantly associated factors were age, ethnicity, place of residence, number of children, refusal of vaccination for themselves, refusal of vaccination for daughters, difficulty talking with daughters about their sexual health, difficulty talking with doctors about their daughters’ sexual health, and the difficulty of bringing up the subject of HPV vaccines. Except for the youngest age group, the majority of daughters’ mothers had positive attitudes toward HPV vaccination. In the youngest age group of daughters’ moth- ers, 65% had neutral attitudes toward HPV vaccination.
The majority of mothers from Almaty (South Kazakhstan) and Oskemen (East Kazakhstan) had positive attitudes, while the majority of mothers from Astana (Capital) and Aktobe (West Kazakhstan) had neutral attitudes toward HPV vaccination. Almost 50% of mothers who refused vaccination for themselves had neutral attitudes toward HPV vaccination, and the majority of mothers who refused vaccination for their daughters (48%) had neutral attitudes toward HPV vaccination. Of all mothers who agreed that it is hard to talk to their daughters about their sexual health, 46% had negative attitudes toward HPV vaccination, while 47% of mothers who confirmed the difficulty bringing up the subject of HPV vaccine had negative attitudes toward HPV vaccination.
Among mothers of sons, 46% had positive attitudes toward HPV vaccination (Table 2). There were no signifi- cant associations with confounding factors possibly due to a small sample size of mothers with male children.
Knowledge and attitude toward HPV infection
The overall level of knowledge about HPV infection and HPV vaccination was low in the sample, with a mean of
Table 1. Socio-demographic characteristics of the study subjects (N = 191).
Variables All mothers N = 191 (%) Mothers with daughters N = 141 Mothers with sons N = 50
Age Mean 37.27 ± 10.06 Mean 37.93 ± 10.25 Mean 35.30 ± 9.34
20–29 49 (26%) 34 (24%) 15 (30%)
30–36 54 (28%) 38 (27%) 16 (32%)
37–45 47 (25%) 36 (26%) 11 (22%)
46 + 41 (21%) 33 (23%) 8 (18%)
Age of having the first child Mean 24.18 ± 4.54 Mean 24.01 ± 4.48 Mean 24.66 ± 4.73 Ethnicity
Kazakh 153 (80%) 118 (84%) 35 (70%)
Other 38 (20%) 23 (16%) 15 (30%)
Highest attained education
Unfinished/finished school 26 (14%) 23 (16%) 3 (6%)
College 62 (32%) 42 (30%) 20 (40%)
University 103 (54%) 76 (54%) 27 (54%)
Place of residence
Astana 43 (23%) 29 (21%) 14 (28%)
Almaty 41 (21%) 34 (24%) 7 (14%)
Aktobe 54 (28%) 41 (29%) 13 (26%)
Oskemen 53 (28%) 37 (26%) 16 (32%)
Household income
Low 91 (48%) 68 (48%) 23 (46%)
Middle 53 (28%) 39 (28%) 14 (28%)
Upper 47 (24%) 34 (24%) 13 (26%)
Marital status
Single 30 (16%) 23 (16%) 7 (14%)
Not single 161 (84%) 118 (84%) 43 (86%)
Children
1–3 children 163 (85%) 114 (81%) 49 (98%)
4 or more children 28 (15%) 27 (19%) 1 (2%)
Children (gender)
Sons only 50 (26%) – 50 (100%)
Daughters or both gender 141 (74%) 141 (100%) –
Refusal of vaccination for themselves
No 117 (61%) 85 (60%) 32 (64%)
Yes 74 (39%) 56 (40%) 18 (36%)
History of abnormal Pap test result
No 160 (84%) 118 (84%) 42 (84%)
Yes 31 (16%) 23 (16%) 8 (16%)
Refusal of vaccination for daughters
No – 76 (55%) –
Yes – 63 (45%) –
Difficulty to talk to my daughter about her sexual health
Disagree – 63 (45%) –
Neutral – 43 (30%) –
Agree – 25 (18%) –
NA 10 (7%) –
Discomfort in discussing my daughter’s sexual health with a doctor or other healthcare professional
Disagree – 71 (50%) –
Neutral – 42 (30%) –
Agree – 19 (14%) –
NA 9 (6%) –
Difficulty bringing up the subject of the HPV vaccine to daughters
Disagree – 63 (45%) –
Neutral – 45 (32%) –
Agree – 20 (14%) –
NA 13 (9%) –
Table 2. Attitude toward HPV vaccination among mothers including social and demographic characteristics, (N = 191). VariablesAll mothers (N = 191)Mothers with daughters (N = 124)Mothers with sons (N = 50) NegativeNeutralPositivep-valueNegativeNeutralPositivep-valueNegativeNeutralPositivep-value 41 (21%)64 (34%)86 (45%)28 (23%)45 (36%)51 (41%)10 (20%)17 (34%)23 (46%) Age 20–299 (18%)21 (43%)19 (39%)p = 0.7652 (7%)19 (65%)8 (28%)p = 0.011*3 (20%)6 (40%)6 (40%)p = 0.708(exact) 30–3614 (26%)15 (28%)25 (46%)11 (32%)7 (21%)16 (47%)3 (19%)6 (37%)7 (44%) 37–459 (19%)15 (32%)23 (49%)8 (27%)8 (27%)14 (46%)1 (9%)4 (36%)6 (55%) 46+9 (22%)13 (32%)19 (46%)7 (23%)11 (35%)13 (42%)3 (38%)1 (12%)4 (50%) Ethnicity Kazakh30 (20%)57 (37%)66 (43%)p = 0.07922 (21%)43 (41%)40 (38%)p = 0.027**7 (20%)14 (40%)14 (40%)p = 0.946(exact) Other11 (29%)7 (18%)20 (53%)6 (32%)2 (10%)11 (58%)3 (20%)3 (20%)9 (60%) Highest attained education Unfinished/finished school9 (35%)11 (42%)6 (23%)p = 0.1334 (29%)8 (57%)2 (14%)p = 0.126(exact)1 (33%)1 (33%)1 (33%)p = 0.802 (exact) College14 (23%)20 (32%)28 (45%)11 (26%)15 (37%)15 (37%)5 (25%)4 (20%)11 (55%) University18 (17%)33 (32%)52 (51%)13 (19%)22 (32%)34 (49%)4 (15%)12 (44%)11 (41%) Place of residence Astana4 (9%)19 (44%)20 (47%)p=0.003*4 (15%)15 (58%)7 (27%)p = 0.003*1 (7%)5 (36%)8 (57%)p = 0.568(exact) Almaty9 (22%)10 (24%)22 (54%)5 (16%)10 (32%)16 (52%)1 (14%)3 (43%)3 (43%) Aktobe10 (19%)26 (48%)18 (33%)8 (21%)18 (46%)13 (33%)4 (31%)5 (38%)4 (31%) Oskemen18 (34%)9 (17%)26 (49%)11 (39%)2 (7%)15 (54%)4 (25%)4 (25%)8 (50%) Household income Low27 (30%)29 (32%)35 (38%)p=0.010*15 (27%)21 (37%)20 (36%)p = 0.7325 (22%)8 (35%)10 (43)%p = 0.845(exact) Middle3 (7%)23 (43%)27 (51%)6 (16%)14 (38%)17 (46%)1 (7%)6 (43%)7 (50%) Upper11 (23%)12 (25%)24 (51%)7 (23%)10 (32%)14 (45%)4 (31%)3 (23%)6 (46%) Marital status Single9 (30%)9 (30%)12 (40%)p = 0.4646 (33.33%)6 (33.33%)6 (33.33%)p = 0.573 exact2 (29%)1 (14%)4 (57%)p = 0.788(exact) Married/in relationship32 (20%)55 (34%)74 (46%)22 (21%)39 (37%)45 (42%)8 (19%)16 (37%)19 (44%) Number of children 1–3 children34 (21%)48 (30%)81 (50%)p = 0.004*19 (19%)33 (33%)47 (48%)p = 0.014*10 (20%)16 (33%)23 (47%)p = 0.978(exact) 4 or more children7 (25%)16 (57%)5 (18%)9 (36%)12 (48%)4 (16%)1 (100%) (Continued)
VariablesAll mothers (N = 191)Mothers with daughters (N = 124)Mothers with sons (N = 50) NegativeNeutralPositivep-valueNegativeNeutralPositivep-valueNegativeNeutralPositivep-value 41 (21%)64 (34%)86 (45%)28 (23%)45 (36%)51 (41%)10 (20%)17 (34%)23 (46%) Child gender Sons only10 (20%)17 (34%)23 (46%)p = 0.957–––––––– Daughters and sons31 (22%)47 (33%)63 (45%)–––––– Refusal of vaccination for themselves No19 (16%)38 (33%)60 (51%)p = 0.038*14 (18%)22 (29%)40 (53%)p = 0.005*6 (19%)12 (38%)14 (44%)p = 0.886(exact) Yes22 (30%)26 (35%)26 (35%)14 (29%)23 (48%)11 (23%)4 (22%)5 (28%)9 (50%) Pap–test history No37 (23%)55 (34%)68 (43%)p = 0.23725 (24%)39 (38%)40 (38%)p = 0.444 exact10 (24%)15 (36%)17 (40%)p = 0.810(exact) Yes4 (13%)9 (29%)18 (58%)3 (15%)6 (30%)11 (55%)2 (25%)6 (75%) Refusal of vaccination for daughters No––––13 (19%)18 (27%)36 (54%)p = 0.007*–––– Yes–––15 (26%)27 (48%)15 (26%)––– Difficulty to talk to my daughter about her sexual health Disagree––––12 (20%)15 (25%)32 (54%)p < 0.001*–––– Neutral–––5 (12%)25 (59%)12 (19%)––– Agree–––11 (46%)6 (25%)7 (29%)––– Discomfort in discussing my daughter’s sexual health with a doctor or other healthcare professional Disagree––––16 (24%)16 (24%)35 (52%)p = 0.004**–––– Neutral–––7 (18%)24 (60%)9 (22%)––– Agree–––5 (29%)5 (29%)7 (42%)––– Difficulty bringing up the subject of the HPV vaccine to daughters Disagree––––12 (20%)13 (22%)35 (58%)p < 0.001**–––– Neutral–––7 (15%)26 (58%)12 (27%)––– Agree–––9 (47%)6 (32%)4 (21%)––– *p value < 0.05, Chi-square test. **p value < 0.05, Fisher’s exact test.
Table 2. (Continued)
2.4 points out of 12 (Figure 1). The median total score is 0 out of 12 for women who have negative and neutral attitudes toward HPV vaccines, while the median score
was 3 points among women with positive attitudes toward HPV vaccines. The upper hinge is lowest among women with neutral attitudes and reaches 4 points among women with negative attitudes, and 6 points among those with positive attitudes toward HPV vaccines. Overall, women with positive attitudes had the highest level of knowl- edge, and those with the least knowledge have neutral attitudes. Attitudes toward HPV vaccination are shown in Figure 2.
Sources of information
The information source about HPV vaccines available for the study participants is shown in Figure 3. Almost 40%
of respondents have their knowledge of HPV vaccination from social media and TV, and 35%—from gynecologists and family physicians (Figure 3). In contrast, the least pop- ular sources of information were pediatricians and schools.
Getting some information regarding the HPV vaccine allowed about half of the women to come to a decision regarding the vaccine, and only 36% of those who came to a decision found it easy (Figure 4).
Figure 1. HPV infection knowledge and attitudes among the study participants.
Figure 2. Attitudes toward HPV vaccines among the study participants.
Figure 3. Source of information about HPV vaccination. Figure 4. Impact of information about HPV vaccines on decision-making about the HPV vaccination.
Discussion
The HPV vaccine is one of the most effective tools for the prevention of cervical cancer,44 a leading cause of death from cancer among women in Kazakhstan.11 The first attempt to implement the HPV vaccination in Kazakhstan in 2013 failed, and the program was discontinued.20–22 In Kazakhstan, parental consent is required for medical inter- ventions for children under 18 years. Parental understand- ing of HPV vaccination’s importance and effectiveness plays a crucial role in their decision-making about the vac- cination of their children. While various factors influence the decision of parents to vaccinate their children,24 moth- ers’ approval and agreement to HPV vaccination is a sig- nificant step to improve vaccination rates.
The failure of previous HPV vaccine attempt confirmed that understanding parental hesitancy and factors that are associated with the attitude of parents toward HPV vacci- nation are crucial for the program’s success. There were no studies that investigated the parental knowledge and atti- tudes to HPV vaccines/vaccination in Kazakhstan. This is the first study in Kazakhstan aimed at understanding the knowledge and attitudes toward HPV vaccination among mothers, and the factors associated with their attitudes.
We also aimed to investigate if differences in attitudes toward HPV vaccination exist according to the gender of their children.
In this study, only 45% of responding mothers had positive attitudes toward HPV vaccination. This level of positive attitudes toward HPV vaccination was similar to the rates established in studies conducted in other upper- middle-income countries. For example, a recent study conducted in China found that parents generally lacked knowledge of HPV and HPV vaccines, yet had moderately high level of intention to vaccinate their children against HPV.45 Similarly, a Romanian study reported that 50.7% of women had a positive attitude toward the vaccine.46
When analyzing female child mothers’ responses, only 41% of responders had positive attitudes toward HPV vac- cination. This was higher than rates in a study conducted in Serbia, where only 25% of parents reported a positive atti- tude.47 According to that study, having daughters and hav- ing more knowledge of HPV were important determinants of a positive attitude toward vaccination among parents of children aged < 9 years.47 A review of the members of the Association of Southeast Asian Nations study showed that parents’ attitudes to HPV vaccines were positive, and most accept the vaccine for their daughters or themselves, even though knowledge about cervical cancer and the HPV vac- cines was poor to moderate.48
Unlike the Serbian study, the factors that were associ- ated with the attitude toward HPV vaccination among mothers in our study were the place of residence, family income, number of children, and history of vaccination refusal for themselves. However, a study about the HPV vaccine in Turkey found that the high economic level,
education, and the employment of the mother had a posi- tive effect on their HPV vaccination attitude.49 According to a Polish study, the only factors linked with the attitude toward HPV vaccination were knowledge and educa- tion.32 Noteworthy in our study was that the level of edu- cation did not affect the attitude of the mother; however, the number of children negatively correlated with the mothers’ attitude.
For mothers of girls, the factors associated with atti- tudes toward HPV vaccination were ethnicity, place of residence, number of children, refusal of vaccination for themselves, and refusal of vaccination for daughters. In particular, difficulty talking with daughters about their sexual health, with doctors about their daughters’ sexual health, and bringing up the subject of the HPV vaccine was associated with negative attitudes toward HPV vaccina- tion. According to Gross at al.,50 mothers’ communication with children about sexually transmitted infections and sexual health is associated with HPV vaccine initiation, and thus positive attitude toward it. As such, the education of mothers, and their ability to communicate with kids openly on these specific topics, plays an important role.
The overall level of knowledge about HPV and HPV vaccination in this study was low. This was in concordance with the recently published UK study, where relatively low levels of knowledge on HPV vaccination were found.51 Similarly, an earlier Italian study found that 83.8% of mothers knew about HPV vaccination before receiving an invitation for vaccination.24 The lowest level of knowledge in this study was seen in women with a neutral attitude toward the vaccine, indicating a potential for a positive shift after the provision of educational information about HPV vaccines. For example, a study among East African mothers has demonstrated a 67% increase in HPV vaccine acceptance after an educational presentation.52
The most common information sources about HPV vac- cination used by mothers in this study were social media, gynecologists, TV, and family doctors. The same findings were reported by the Italian study on the knowledge and attitudes of Italian mothers toward HPV vaccination.24 The importance of the doctor’s recommendation was estab- lished earlier,53 and is one of the main differences between parents of boys and girls.54,55 However, in our study, no sig- nificant difference was found between mothers of boys and girls. This might be a reflection of the general lack of HPV vaccine promotion in the country, which results in equally low levels of awareness and knowledge in the population.
Study strengths and limitations
The main strength of this study is that it provides infor- mation on mothers’ attitudes toward HPV vaccination in Kazakhstan. Moreover, the study covered geographically distant populations of the country. In a light of planned relaunching of the HPV vaccination program in Kazakhstan, understanding of the mothers’ attitudes toward HPV
vaccination will contribute to the development of the information campaign. We also acknowledge some limi- tations presented in the study. Since a relatively small sample of mothers attending gynecological clinics was recruited, the study results might not be generalizable to the general population of Kazakhstani mothers. Moreover, there is the possibility that healthy volunteer bias is pre- sent, as women who agree to participate in studies could be more favorable toward vaccination than those who refused to participate. Thus, the results are based on the selected study population. Unfortunately, we do not have access to data to compare the characteristics of the study respondents to non-respondents to assess for possible non-response bias. Another limitation is that the questions measuring the attitude construct were not tested or vali- dated previously in Kazakhstan. Finally, fathers were not included in the study. Thus, the study findings are only relevant to mothers. However, it would be interesting and important to investigate fathers’ attitudes as well.
Generalizability
Although this study included participants from different regions of Kazakhstan (four large cities), the generalizabil- ity of the study results could be limited due to the relative small number of participants. Moreover, this study find- ings may not be appropriate for the rural area population as only urban residents (attendee of gynecological clinics) were enrolled.
Conclusion
Mothers play a significant role in decision-making about HPV vaccination for their children. Relatively low posi- tive attitudes toward HPV vaccination were found among mothers in general and mothers of female children in par- ticular. It is evident that informational interventions are needed for women who are less likely to accept the vacci- nation for their daughters. Understanding different factors associated with attitudes toward HPV vaccination should help address barriers to HPV vaccination before the national HPV vaccination program will start in Kazakhstan.
Moreover, this study’s findings will help to create cultur- ally appropriate educational campaigns that should work to improve mothers’ opinions about HPV vaccination.
Declarations
Ethics approval and consent to participate
The study was approved by the Institutional Research Ethics Committee (IREC) of the Nazarbayev University on April 23, 2019 (IREC number: 146/4042019). After the explanation of the voluntary and anonymous nature of the study, verbal consent was obtained from all study participants.
The study was conducted in compliance with the Declaration of Helsinki and was approved by the Institutional Research Ethics
Committee (IREC) of Nazarbayev University on April 23, 2019 (IREC number: 146/4042019). All participants were informed about the aims, methods, risks, and benefits of the study prior to participation in the study. After the explanation of the voluntary and anonymous nature of the study, verbal consent was obtained from the study participants. The verbal consent was considered the most appropriate to fulfill the anonymous nature of the study.
Moreover, the choice of verbal consent was dictated by the cul- tural context of Kazakhstan as a post-Soviet country, where peo- ple are not comfortable with “signing documents that are similar to a contract.” Verbal consent used for this study included all the necessary components for informed consent (Appendix C, Verbal Consent). No personal information related to any of the partici- pants was available to the research team. The statements on the study participants’ rights were declared orally and in the informa- tion letter provided to the participants.
Consent for publication Not applicable
Author contribution(s)
Aisha Babi: Data curation; Formal analysis; Methodology;
Software; Validation; Writing—original draft; Writing—review
& editing.
Torgyn Issa: Software; Supervision; Validation; Visualization;
Writing—original draft; Writing—review & editing.
Alpamys Issanov: Conceptualization; Data curation; Formal analysis; Methodology; Software; Writing—original draft;
Writing—review & editing.
Sholpan Akhanova: Data curation; Formal analysis; Investi- gation; Writing—original draft.
Natalya Udalova: Data curation; Formal analysis; Investigation;
Resources; Writing—original draft.
Svetlana Koktova: Data curation; Investigation; Resources;
Validation; Writing—review & editing.
Askhat Balykov: Conceptualization; Data curation; Investiga- tion; Resources; Supervision; Writing—review & editing.
Zhanna Sattarkyzy: Data curation; Investigation; Resources;
Supervision; Visualization; Writing—review & editing.
Balkenzhe Imankulova: Data curation; Formal analysis;
Investigation; Resources; Writing—review & editing.
Nazira Kamzayeva: Data curation; Investigation; Supervision;
Writing—review & editing.
Wassim Y. Almawi: Conceptualization; Project administration;
Visualization; Writing—original draft; Writing—review &
editing.
Gulzhanat Aimagambetova: Conceptualization; Data curation;
Investigation; Methodology; Project administration; Resources;
Supervision; Validation; Visualization; Writing—original draft;
Writing—review & editing.
Acknowledgements
The authors would like to acknowledge the School of Medicine, Nazarbayev University for the continuous support that enabled completion of this study.
Funding
The author(s) received no financial support for the research, authorship, and/or publication of this article.
Competing interests
The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
Availability of data and materials
All data related to this study are available from the authors ([email protected]) upon reasonable request and with permission of the NU IREC.
ORCID iDs
Aisha Babi https://orcid.org/0000-0002-2726-6955 Torgyn Issa https://orcid.org/0000-0001-5214-6691 Alpamys Issanov https://orcid.org/0000-0002-8968-2655 Sholpan Akhanova https://orcid.org/0000-0002-9408-0640 Natalya Udalova https://orcid.org/0000-0003-3259-9719 Svetlana Koktova https://orcid.org/0009-0007-5140-6667 Askhat Balykov https://orcid.org/0009-0001-7463-7413 Zhanna Sattarkyzy https://orcid.org/0009-0002-7455-1924 Balkenzhe Imankulova https://orcid.org/0000-0001-8124-5517 Nazira Kamzayeva https://orcid.org/0009-0009-0229-2661 Wassim Y Almawi https://orcid.org/0000-0003-1633-9757 Gulzhanat Aimagambetova https://orcid.org/0000-0002-2868 -4497
Supplemental material
Supplemental material for this article is available online.
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