Knowledge and attitudes of mothers toward HPV vaccination: A cross-sectional study in Kazakhstan

Abstract

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

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 prevalence 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 cancer.^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 recognized.^12,14,15 The effectiveness of the HPV vaccination was also demonstrated by the drastic reduction in cervical 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 parents.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 living 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 relatives.^27,28 In families where mothers were decision-makers 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 children’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 education.^31,32 The politicization of information about HPV vaccines causes increased confusion and likely negative emotional response.³³ On the other hand, providing relevant medical information increases acceptance of the HPV vaccine.³⁴ It is important to establish the contribution 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 following 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 languages officially used for communication in the Republic of Kazakhstan). Women younger than 18 years, those without 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 participation 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 questionnaire. The response rate was 55%.

Study instrument

The study instrument was a paper-based survey composed 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-translated into Kazakh and Russian languages with the help of independent trilingual (English-Russian-Kazakh) interpreters. 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 translation, back translation, expert committee review, and testing of the version. Discrepancies in translations/interpretations 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 information 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 bringing 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 demonstrated 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 negative (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 correct 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 attitudes at 50%. The suggested sample size was 384.

Ethical considerations

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 study 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 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 information 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 performed 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 ethnicity (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 children, 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.

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 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 attitudes toward HPV vaccination. Except for Aktobe, where most participants had neutral attitudes toward HPV vaccination. Irrespective of family income, most mothers had positive attitudes toward HPV vaccination, and half of the mothers (51%) had positive attitudes toward HPV vaccination. 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 vaccination 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.

Table 2.

Attitude toward HPV vaccination among mothers including social and demographic characteristics, (N = 191).

Variables	All mothers (N = 191)				Mothers with daughters (N = 124)				Mothers with sons (N = 50)
	Negative	Neutral	Positive	p-value	Negative	Neutral	Positive	p-value	Negative	Neutral	Positive	p-value
	41 (21%)	64 (34%)	86 (45%)		28 (23%)	45 (36%)	51 (41%)		10 (20%)	17 (34%)	23 (46%)
Age
20–29	9 (18%)	21 (43%)	19 (39%)	p = 0.765	2 (7%)	19 (65%)	8 (28%)	p = 0.011*	3 (20%)	6 (40%)	6 (40%)	p = 0.708(exact)
30–36	14 (26%)	15 (28%)	25 (46%)		11 (32%)	7 (21%)	16 (47%)		3 (19%)	6 (37%)	7 (44%)
37–45	9 (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
Kazakh	30 (20%)	57 (37%)	66 (43%)	p = 0.079	22 (21%)	43 (41%)	40 (38%)	p = 0.027**	7 (20%)	14 (40%)	14 (40%)	p = 0.946(exact)
Other	11 (29%)	7 (18%)	20 (53%)		6 (32%)	2 (10%)	11 (58%)		3 (20%)	3 (20%)	9 (60%)
Highest attained education
Unfinished/finished school	9 (35%)	11 (42%)	6 (23%)	p = 0.133	4 (29%)	8 (57%)	2 (14%)	p = 0.126(exact)	1 (33%)	1 (33%)	1 (33%)	p = 0.802 (exact)
College	14 (23%)	20 (32%)	28 (45%)		11 (26%)	15 (37%)	15 (37%)		5 (25%)	4 (20%)	11 (55%)
University	18 (17%)	33 (32%)	52 (51%)		13 (19%)	22 (32%)	34 (49%)		4 (15%)	12 (44%)	11 (41%)
Place of residence
Astana	4 (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)
Almaty	9 (22%)	10 (24%)	22 (54%)		5 (16%)	10 (32%)	16 (52%)		1 (14%)	3 (43%)	3 (43%)
Aktobe	10 (19%)	26 (48%)	18 (33%)		8 (21%)	18 (46%)	13 (33%)		4 (31%)	5 (38%)	4 (31%)
Oskemen	18 (34%)	9 (17%)	26 (49%)		11 (39%)	2 (7%)	15 (54%)		4 (25%)	4 (25%)	8 (50%)
Household income
Low	27 (30%)	29 (32%)	35 (38%)	p = 0.010*	15 (27%)	21 (37%)	20 (36%)	p = 0.732	5 (22%)	8 (35%)	10 (43)%	p = 0.845(exact)
Middle	3 (7%)	23 (43%)	27 (51%)		6 (16%)	14 (38%)	17 (46%)		1 (7%)	6 (43%)	7 (50%)
Upper	11 (23%)	12 (25%)	24 (51%)		7 (23%)	10 (32%)	14 (45%)		4 (31%)	3 (23%)	6 (46%)
Marital status
Single	9 (30%)	9 (30%)	12 (40%)	p = 0.464	6 (33.33%)	6 (33.33%)	6 (33.33%)	p = 0.573 exact	2 (29%)	1 (14%)	4 (57%)	p = 0.788(exact)
Married/in relationship	32 (20%)	55 (34%)	74 (46%)		22 (21%)	39 (37%)	45 (42%)		8 (19%)	16 (37%)	19 (44%)
Number of children
1–3 children	34 (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 children	7 (25%)	16 (57%)	5 (18%)		9 (36%)	12 (48%)	4 (16%)			1 (100%)
Child gender
Sons only	10 (20%)	17 (34%)	23 (46%)	p = 0.957	–	–	–	–	–	–	–	–
Daughters and sons	31 (22%)	47 (33%)	63 (45%)		–	–	–		–	–	–
Refusal of vaccination for themselves
No	19 (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)
Yes	22 (30%)	26 (35%)	26 (35%)		14 (29%)	23 (48%)	11 (23%)		4 (22%)	5 (28%)	9 (50%)
Pap–test history
No	37 (23%)	55 (34%)	68 (43%)	p = 0.237	25 (24%)	39 (38%)	40 (38%)	p = 0.444 exact	10 (24%)	15 (36%)	17 (40%)	p = 0.810(exact)
Yes	4 (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.

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’ mothers, 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 significant 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 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 knowledge, and those with the least knowledge have neutral attitudes. Attitudes toward HPV vaccination are shown in Figure 2.

Figure 1.

HPV infection knowledge and attitudes among the study participants.

Figure 2.

Attitudes toward HPV vaccines among the study participants.

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 popular 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 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 interventions for children under 18 years. Parental understanding of HPV vaccination’s importance and effectiveness plays a crucial role in their decision-making about the vaccination of their children. While various factors influence the decision of parents to vaccinate their children,²⁴ mothers’ approval and agreement to HPV vaccination is a significant 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 vaccination are crucial for the program’s success. There were no studies that investigated the parental knowledge and attitudes 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 vaccination. This was higher than rates in a study conducted in Serbia, where only 25% of parents reported a positive attitude.⁴⁷ According to that study, having daughters and having 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 vaccines was poor to moderate.⁴⁸

Unlike the Serbian study, the factors that were associated 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 positive 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 education.³² Noteworthy in our study was that the level of education 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 attitudes 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 vaccination. 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 vaccination 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 established earlier,⁵³ and is one of the main differences between parents of boys and girls.^54,55 However, in our study, no significant 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 information 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 limitations 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 present, 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 validated 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 generalizability of the study results could be limited due to the relative small number of participants. Moreover, this study findings 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 positive attitudes toward HPV vaccination were found among mothers in general and mothers of female children in particular. It is evident that informational interventions are needed for women who are less likely to accept the vaccination 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 culturally appropriate educational campaigns that should work to improve mothers’ opinions about HPV vaccination.

Supplemental Material

sj-docx-1-whe-10.1177_17455057231172355 – Supplemental material for Knowledge and attitudes of mothers toward HPV vaccination: A cross-sectional study in Kazakhstan

Supplemental material, sj-docx-1-whe-10.1177_17455057231172355 for Knowledge and attitudes of mothers toward HPV vaccination: A cross-sectional study in Kazakhstan by Aisha Babi, Torgyn Issa, Alpamys Issanov, Sholpan Akhanova, Natalya Udalova, Svetlana Koktova, Askhat Balykov, Zhanna Sattarkyzy, Balkenzhe Imankulova, Nazira Kamzayeva, Wassim Y. Almawi and Gulzhanat Aimagambetova in Women's Health

Supplemental Material

sj-docx-2-whe-10.1177_17455057231172355 – Supplemental material for Knowledge and attitudes of mothers toward HPV vaccination: A cross-sectional study in Kazakhstan

Supplemental material, sj-docx-2-whe-10.1177_17455057231172355 for Knowledge and attitudes of mothers toward HPV vaccination: A cross-sectional study in Kazakhstan by Aisha Babi, Torgyn Issa, Alpamys Issanov, Sholpan Akhanova, Natalya Udalova, Svetlana Koktova, Askhat Balykov, Zhanna Sattarkyzy, Balkenzhe Imankulova, Nazira Kamzayeva, Wassim Y. Almawi and Gulzhanat Aimagambetova in Women's Health

Supplemental Material

sj-docx-3-whe-10.1177_17455057231172355 – Supplemental material for Knowledge and attitudes of mothers toward HPV vaccination: A cross-sectional study in Kazakhstan

Supplemental material, sj-docx-3-whe-10.1177_17455057231172355 for Knowledge and attitudes of mothers toward HPV vaccination: A cross-sectional study in Kazakhstan by Aisha Babi, Torgyn Issa, Alpamys Issanov, Sholpan Akhanova, Natalya Udalova, Svetlana Koktova, Askhat Balykov, Zhanna Sattarkyzy, Balkenzhe Imankulova, Nazira Kamzayeva, Wassim Y. Almawi and Gulzhanat Aimagambetova in Women's Health

Footnotes

Acknowledgements

The authors would like to acknowledge the School of Medicine, Nazarbayev University for the continuous support that enabled completion of this study.

Declarations

ORCID iDs

Aisha Babi

Torgyn Issa

Alpamys Issanov

Sholpan Akhanova

Natalya Udalova

Svetlana Koktova

Askhat Balykov

Zhanna Sattarkyzy

Balkenzhe Imankulova

Nazira Kamzayeva

Wassim Y Almawi

Gulzhanat Aimagambetova

Supplemental material

Supplemental material for this article is available online.

References

World Health Organization. Human Papillomavirus (HPV), 2022, https://www.who.int/teams/health-product-policy-and-standards/standards-and-specifications/vaccine-standardization/human-papillomavirus (accessed on 13 April 2022).

Zur Hausen

. Papillomaviruses in the causation of human cancers—a brief historical account. Virology 2009; 384(2): 260–265.

Arbyn

Weiderpass

Bruni

, et al. Estimates of incidence and mortality of cervical cancer in 2018: a worldwide analysis [published correction appears in Lancet Glob Health. 2022 Jan;10(1):e41]. Lancet Glob Health 2020; 8(2): e191–e203.

Rogovskaya

Shabalova

Mikheeva

, et al. Human papillomavirus prevalence and type-distribution, cervical cancer screening practices and current status of vaccination implementation in Russian Federation, the Western countries of the former Soviet Union, Caucasus region and Central Asia. Vaccine 2013; 31(Suppl. 7): H46–H58.

Bekmukhambetov

Balmagambetova

Jarkenov

, et al. Distribution of high risk human papillomavirus types in Western Kazakhstan—retrospective analysis of PCR data. Asian Pac J Cancer Prev 2016; 17(5): 2667–2672.

Niyazmetova

Aimagambetova

Stambekova

, et al. Application of molecular genotyping to determine prevalence of HPV strains in Pap smears of Kazakhstan women. Int J Infect Dis 2017; 54: 85–88.

Babi

Issa

Issanov

, et al. Prevalence of high-risk human papillomavirus infection among Kazakhstani women attending gynecological outpatient clinics. Int J Infect Dis 2021; 109: 8–16.

Aimagambetova

Babi

Issanov

, et al. The distribution and prevalence of high-risk HPV genotypes other than HPV-16 and HPV-18 among women attending gynecologists’ offices in Kazakhstan. Biology 2021; 10(8): 794.

Aimagambetova

Azizan

Epidemiology of HPV infection and HPV-related cancers in Kazakhstan: a review. Asian Pac J Cancer Prev 2018; 19(5): 1175–1180.

10.

Aimagambetova

Chan

Ukybassova

, et al. Cervical cancer screening and prevention in Kazakhstan and Central Asia. J Med Screen 2021; 28(1): 48–50.

11.

Bruni

Albero

Serrano

, et al. ICO/IARC information centre on HPV and cancer (HPV Information Centre). Human Papillomavirus and Related Diseases in Kazakhstan. Summary Report 07 March 2023. https://hpvcentre.net/statistics/reports/KAZ.pdf

12.

Akhatova

Azizan

Atageldiyeva

, et al. Prophylactic human papillomavirus vaccination: from the origin to the current state. Vaccines(Basel) 2022; 10(11): 1912.

13.

World Health Organization. Global strategy to accelerate the elimination of cervical cancer as a public health problem. Geneva, http://apps.who.int/bookorders (accessed on 30 April 2022).

14.

Centers for Disease Control Prevention (CDC). Reasons to get HPV vaccine, https://www.cdc.gov/hpv/parents/vaccine/six-reasons.html (accessed on 18 April 2022).

15.

Tabrizi

Brotherton

Kaldor

, et al. Assessment of herd immunity and cross-protection after a human papillomavirus vaccination programme in Australia: a repeat cross-sectional study. Lancet Infect Dis 2014; 14(10): 958–966.

16.

Pollock

Kavanagh

Potts

, et al. Reduction of low- and high-grade cervical abnormalities associated with high uptake of the HPV bivalent vaccine in Scotland. Br J Cancer 2014; 111(9): 1824–1830.

17.

Luostarinen

Apter

Dillner

, et al. Vaccination protects against invasive HPV-associated cancers. Int J Cancer 2018; 142(10): 2186–2187.

18.

Kjaer

Dehlendorff

Belmonte

, et al. Real-world effectiveness of human papillomavirus vaccination against cervical cancer. J Natl Cancer Inst 2021; 113(10): 1329–1335.

19.

Issanov

Karim

Aimagambetova

, et al. Does vaccination protect against human papillomavirus-related cancers? Preliminary findings from the United States national health and nutrition examination survey (2011-2018). Vaccines(Basel) 2022; 10(12): 2113.

20.

Issa

Babi

Issanov

, et al. Knowledge and awareness of human papillomavirus infection and human papillomavirus vaccine among Kazakhstani women attending gynecological clinics. PLoS ONE 2021; 16(12): e0261203.

21.

Aimagambetova

Babi

Issa

, et al. What factors are associated with attitudes towards HPV vaccination among Kazakhstani women? Exploratory analysis of cross-sectional survey data. Vaccines(Basel) 2022; 10(5): 824.

22.

Kaidarova

Chingissova

Dushimova

, et al. Implementation of HPV vaccination pilot project in Kazakhstan: successes and challenges. J Clin Oncol 2019; 37(15_suppl): e13056.

23.

Hanley

Yoshioka

Ito

, et al. HPV vaccination crisis in Japan [published correction appears in Lancet. 2015 Jul 18;386(9990):248]. Lancet 2015; 385(9987): 2571.

24.

La Torre

De Vito

Ficarra

, et al. Knowledge, opinions and attitudes of Italian mothers towards HPV vaccination and Pap test. Tumori 2015; 101(3): 339–346.

25.

Szilagyi

Albertin

Gurfinkel

, et al. Prevalence and characteristics of HPV vaccine hesitancy among parents of adolescents across the US. Vaccine 2020; 38(38): 6027–6037.

26.

Sonawane

Zhu

Montealegre

, et al. Parental intent to initiate and complete the human papillomavirus vaccine series in the USA: a nationwide, cross-sectional survey. Lancet Public Health 2020; 5(9): e484–e492.

27.

Luman

McCauley

Shefer

, et al. Maternal characteristics associated with vaccination of young children. Pediatrics 2003; 111(5 Pt. 2): 1215–1218.

28.

Sythes

Bedford

Motherhood and vaccine refusal in the United Kingdom: a new examination of gender, identity and the journey to contemporary non-vaccination. Child Care Health Dev 2022; 48(6): 979–989.

29.

Jalloh

Sengeh

Ibrahim

, et al. Association of community engagement with vaccination confidence and uptake: a cross-sectional survey in Sierra Leone, 2019. J Glob Health 2022; 12: 04006.

30.

Karafillakis

Peretti-Watel

Verger

, et al. ‘I trust them because my mum trusts them’: exploring the role of trust in HPV vaccination decision-making among adolescent girls and their mothers in France. Vaccine 2022; 40(8): 1090–1097.

31.

Azh

Hosseinzadeh

Javadi

, et al. Factors predicting mothers’ intention toward human papilloma virus vaccination of adolescents: a cross-sectional study among Iranian Families. Iran J Nurs Midwifery Res 2021; 26(6): 495–499.

32.

Smolarczyk

Duszewska

Drozd

, et al. Parents’ knowledge and attitude towards HPV and HPV vaccination in Poland. Vaccines(Basel) 2022; 10(2): 228.

33.

Fowler

Nagler

Banka

, et al. Effects of politicized media coverage: experimental evidence from the HPV vaccine and COVID-19. Prog Mol Biol Transl Sci 2022; 188(1): 101–134.

34.

Mizumachi

Aoki

Kitano

, et al. How to recover lost vaccine acceptance? A multi-center survey on HPV vaccine acceptance in Japan. J Infect Chemother 2021; 27(3): 445–449.

35.

Dib

Mayaud

Launay

, et al. Design and content validation of a survey questionnaire assessing the determinants of human papillomavirus (HPV) vaccine hesitancy in France: a reactive Delphi study. Vaccine 2020; 38(39): 6127–6140.

36.

Beaton

Bombardier

Guillemin

, et al. Guidelines for the process of cross-cultural adaptation of self-report measures. Spine 2000; 25(24): 3186–3191.

37.

Sousa

Rojjanasrirat

Translation, adaptation and validation of instruments or scales for use in cross-cultural health care research: a clear and user-friendly guideline. J Eval Clin Pract 2011; 17(2): 268–274.

38.

Hilton

Skrutkowski

Translating instruments into other languages: development and testing processes. Cancer Nurs 2002; 25(1): 1–7.

39.

Bureau of National Statistics. Agency for Strategic planning reforms of the Republic of Kazakhstan, https://www.stat.gov.kz/ (accessed on 20 February 2022).

40.

Askelson

Campo

Lowe

, et al. Using the theory of planned behavior to predict mothers’ intentions to vaccinate their daughters against HPV. J Sch Nurs 2010; 26(3): 194–202.

41.

Jamieson

Likert scales: how to (ab)use them. Med Educ 2004; 38(12): 1217–1218.

42.

Dean

Sullivan

Soe

. OpenEpi: open source epidemiologic statistics for public health, Version. www.OpenEpi.com, https://www.openepi.com/Menu/OE_Menu.htm

43.

StataCorp LLC. Stata Statistical Software: Release 16, 2019, https://www.stata.com/support/faqs/resources/citing-software-documentation-faqs/#:~:text=2019., Station%2C TX%3A StataCorp LLC.&text=StataCorp.,-2017

44.

Canfell

Towards the global elimination of cervical cancer. Papillomavirus Res 2019; 8: 100170.

45.

Zhu

Zhai

Siu

, et al. Factors related to Chinese parents’ HPV vaccination intention for children. Am J Health Behav 2019; 43(5): 994–1005.

46.

Grigore

Teleman

Pristavu

, et al. Awareness and knowledge about HPV and HPV vaccine among Romanian women. J Cancer Educ 2018; 33(1): 154–159.

47.

Marić

Birčanin

Kisić

, et al. Parental perspective on human papillomavirus (HPV) vaccination in Serbia: knowledge, attitudes and practice. Sex Reprod Healthc 2018; 16: 192–198.

48.

Wijayanti

Schütze

MacPhail

, et al. Parents’ knowledge, beliefs, acceptance and uptake of the HPV vaccine in members of the association of Southeast Asian Nations (ASEAN): a systematic review of quantitative and qualitative studies. Vaccine 2021; 39(17): 2335–2343.

49.

Özdemir

Akkaya

Karaşahin

KE.

Analysis of community-based studies related with knowledge, awareness, attitude, and behaviors towards HPV and HPV vaccine published in Turkey: a systematic review. J Turk Ger Gynecol Assoc 2020; 21(2): 111–123.

50.

Gross

Laz

Rahman

, et al. Association between mother-child sexual communication and HPV vaccine uptake. Prev Med 2015; 74: 63–66.

51.

Taylor

Nailer

Cohen

, et al. HPV vaccination and cervical screening: the knowledge and attitudes of mothers of adolescent girls. Psychol Health. Epub ahead of print 2 June 2022. DOI: 10.1080/08870446.2022.2081327.

52.

Chu

Ibrahim

, et al. The impact of an educational forum intervention on East African mothers’ HPV vaccine-related knowledge, attitudes, and intentions to vaccinate their adolescent children. Vaccine 2021; 39(28): 3767–3776.

53.

López

Garcés-Sánchez

Panizo

, et al. HPV knowledge and vaccine acceptance among European adolescents and their parents: a systematic literature review [published correction appears in Public Health Rev. 2020 Jul 21;41:20]. Public Health Rev 2020; 41: 10.

54.

Lindley

Jeyarajah

Yankey

, et al. Comparing human papillomavirus vaccine knowledge and intentions among parents of boys and girls. Hum Vaccin Immunother 2016; 12(6): 1519–1527.

55.

Gilkey

Moss

McRee

, et al. Do correlates of HPV vaccine initiation differ between adolescent boys and girls? Vaccine 2012; 30(41): 5928–5934.

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