The association between maternal human papillomavirus (HPV) experiences and HPV vaccination of their children

ABSTRACT

HPV vaccination prevents most HPV-related cancers yet vaccination rates remain low. In this cross-sectional study, we examined the association between maternal HPV experiences and HPV vaccination uptake among children and whether this association may be explained by perceived benefits of vaccination. We used logistic regression models to estimate the effect of (1) maternal history of abnormal Pap smear, (2), family/friend history of cervical cancer, and (3) maternal history of cervical cancer on HPV vaccination uptake among children. Separate mediation analyses were conducted to determine if perceived benefits mediated the relationship between each maternal HPV experience and HPV vaccination uptake. History of abnormal Pap smear (OR = 1.50, 95% CI = 1.15, 1.97), family history of cervical cancer (OR = 1.72, CI = 1.26, 2.35), and personal history of cervical cancer (OR = 3.00, CI = 1.82, 4.95) predicted HPV vaccination of children. Perceived benefits mediated the relationship between history of abnormal Pap smear (indirect effect =.146, SE =.069, 95% CI =.014, .289), family history of cervical cancer (indirect effect =.228, SE =.079, CI =.080, .387), and personal history of cervical cancer (indirect effect =.298, SE =.116, CI =.082, .533) on HPV vaccination. Our results suggest that personal experiences with HPV-related disease may influence maternal HPV vaccine decision-making.

KEYWORDS:

• Human papillomavirus (HPV) vaccination
• cervical cancer history
• perceived benefits

Introduction

Approximately 70% of human papillomavirus (HPV)-related cancers (including cervical, oropharyngeal, anal, penile, and vulvar cancers) are preventable through widespread HPV vaccination.¹ In 2018, however, only 62.6% of children received at least one dose of the vaccination by age 13. This suboptimal HPV vaccination rate puts children at risk for HPV-related disease.² The United States (US) Advisory Committee on Immunization Practices (ACIP) recommends routine vaccination for all children at ages 11–12 y and routine catch-up vaccination for all persons ages 13–26.³ Vaccination may be initiated at ages 9 or 10. When the first dose is administered before age 15, only two doses are required, 6–12 months apart. Parents, particularly mothers, play a key role in HPV vaccination decision-making and education about the HPV vaccine with their children.^4,5

HPV vaccine uptake with daughters has been associated with maternal HPV experiences, including personal history of abnormal Papanicolaou (Pap) smear^6,7 and family/friend history of cervical cancer.⁷ Previous studies, however, have rarely examined the relationship between maternal HPV experiences (e.g. personal history of abnormal Pap smears or cervical cancer or family/friend cervical cancer history) and HPV vaccine uptake (i.e., receipt of at least one dose) among both daughters and sons.⁷ Previous studies have also not examined factors such as perceived benefits that may explain the relationship between maternal HPV experiences and HPV vaccination in children according to behavioral theory.^8–10 Perceived benefits is a concept from the Health Behavior Model (HBM)¹¹ that is used in behavioral interventions to increase cancer screenings¹² and vaccine use¹³ but has been used less in interventions specifically targeting HPV vaccination uptake. Perceived benefits should be theoretically linked to the behavior of HPV vaccination, as noted by previous studies.^5,14 Personal HPV-experiences among mothers or female guardians may lead them to value HPV vaccination and see greater benefits to vaccination, increasing the likelihood of HPV vaccination of their children, compared to women who have not had such experiences. Other factors that may be related to vaccine uptake include maternal age,⁷ income,⁸ child’s age,⁹ and child’s sex.¹⁰

The purpose of this cross-sectional study was to examine (a) the relationship between maternal HPV experiences and sociodemographic characteristics (maternal age, income, child’s age, and child’s sex) with HPV vaccine uptake among children and (b) whether maternal perceived benefits of HPV vaccination explained the relationship between maternal HPV experiences and vaccine uptake while controlling for sociodemographic covariates. The current study could inform future interventions to increase HPV vaccination of children aimed at mothers who never had personal HPV experiences by including narratives about potential adverse effects of non-vaccination and benefits of HPV vaccination.

Methods

Study design

Cross-sectional data were collected in August 2014 by Survey Sampling International (SSI – now called Dynata), a survey research company that maintains a panel of over 4 million individuals in the United States. The data used for the present analyses were from a larger HPV vaccine and flu vaccine health messaging intervention survey study.¹⁵ The IRB at Indiana University approved the protocol and categorized this research as exempt.

E-mail invitations were sent at random by SSI to the target mothers or female legal guardians (aged 18–81) of 9–13-year-old children living in their households. Panelists responded to the study invitation by clicking a link to a web-based survey through Qualtrics (Qualtrics, Provo, Utah). After reading a brief description of the study, women decided whether to participate. To be eligible to complete the survey, participants had to be (a) the mother or female legal guardian of a 9–13-year-old child living in the US, (b) at least 18 years of age, and c) able to read and write English. Participants were asked to respond regarding their youngest child if a mother had more than one child in the 9–13 age range. One hundred sixty-eight women reported never having a Pap smear and were therefore excluded from analyses with the history of abnormal Pap smear variable.

Measures

Participants (n = 1155) provided sociodemographic and other health-related information, including mother’s age, income, child’s age, child’s sex, and doses of HPV vaccine the child had received (1 or more vs. none). Variables measuring HPV experiences (yes/no) included (1) ever received abnormal results from a Pap smear, (2) ever had a family member or close friend who has been diagnosed with cervical cancer, and (3) ever been diagnosed with cervical cancer.

Perceived benefits of HPV vaccination were measured with the following five items, reported on a 5-point Likert scale (Cronbach’s alpha = .92): “The HPV vaccine is the best way to protect my child from HPV infection”; “The HPV vaccine is effective in preventing genital warts, cervical cancer, and anal cancer”; “The HPV vaccine is safe”; “It is important for the health of everyone for parents to vaccinate their children against HPV”; and “A vaccine could be a good way to protect my child from HPV infection.” The scale has been shown to have predictive validity in previous research related to HPV vaccination uptake.¹⁶ A higher perceived benefits score corresponded to a higher level of perceived benefits of vaccination. The outcome variable was HPV vaccination uptake, measured by whether or not a participant’s child had received at least one dose of the HPV vaccine.

Data analysis

We conducted all analyses in SPSS Version 25 (IBM SPSS, Chicago, Ill). Descriptive statistics were used to analyze sociodemographics, maternal experiences, and HPV vaccine uptake. Bivariate analyses including chi-square tests between categorical variables and t-tests between continuous and categorical variables were conducted. Odds ratios (ORs) and 95% confidence intervals (CIs) (p < .005) were calculated between each sociodemographic and maternal experience variable and HPV vaccine uptake.

Mediation was tested by using the Hayes PROCESS macro procedure for SPSS.¹⁷ Mediation was tested using Model 4 in PROCESS by examining perceived benefits as a mediator between each maternal experience (history of abnormal Pap smear, family/friend with cervical cancer, and personal history of cervical cancer) and HPV vaccination uptake while controlling for covariates (maternal age, income, child’s age, and child’s sex).¹⁷ Bootstrapping with 5,000 resamples was used for all mediation analyses.

Results

Demographics and health-related characteristics

Demographic and health-related characteristics of the sample are described in Table 1 and include HPV vaccination uptake (1 or more vs none), child’s age, child’s sex, mother’s age, income, ever receiving abnormal Pap smear results, having a family member or close friend who had been diagnosed with cervical cancer, and ever personally being diagnosed with cervical cancer. More details regarding the sociodemographic characteristics of the sample have been described elsewhere.¹⁵ Most of the children had not received any doses of the HPV vaccine (64%). The average of female children was 10.68 and 10.63 for males. Fifty percent of children were between the ages of 9–10 y, and most were female (59%). The average age of mothers was 37.5. Most (52%) mothers were in the 25,000 USD-$74,999 income range. An abnormal Pap smear history was reported by 36% of participants, while a minority of participants (18%) indicated that a family member or close friend had been diagnosed with cervical cancer. Six percent reported ever having been diagnosed with cervical cancer.

Table 1. Descriptive and bivariate logistic results

	X (SD) or % (N)	HPV vaccination uptake (1 or more doses)	OR (95% CI)
Child received 1 or more doses of HPV vaccine Yes No	396 (36%) 701 (64%)
Child’s age 9–10 years old 11–13 years old	50% (594) 50% (588)	41% (162) 59% (234)	ref 1.75 (1.36, 2.24)
Child’s sex Female Male	59% (702) 41% (482)	64% (255) 36% (141)	1.31 (1.02, 1.70) ref
Maternal age	37.5 (8.033)	37.7 (7.801)	.98 (.96,.99)
Income $24,999 or less $25,000-$74,999 $75,000 or more	17% (187) 52% (589) 31% (347)	18% (67) 51% (193) 31% (119)	ref.79 (.55, 1.13).79 (.54, 1.17)
Maternal history of abnormal Pap smear Yes No	36% (384) 64% (684)	42% (144) 58% (195)	1.50 (1.15, 1.97) ref
Family/friend history of cervical cancer Yes No	18% (211) 82% (935)	24% (92) 76% (290)	1.72 (1.26, 2.35) ref
Maternal history of cervical cancer Cervical cancer diagnosis Never diagnosed	6% (70) 94% (1085)	11% (42) 89% (342)	3.00 (1.82, 4.95) ref

Abbreviations:X = mean, SD = Standard Deviation, N = number, OR = Odds Ratio, CI = Confidence Interval

Bivariate results between sociodemographics and maternal experiences to children’s HPV vaccination uptake are described in Table 1. The majority of children who were vaccinated were between the ages of 11–13 y (59%) and female (60%). The average age of mothers who vaccinated their children was 37.7, and most who vaccinated were in the 25,000 USD-$74,999 income range. Among children who received an HPV vaccination, 42% of mothers had a history of abnormal Pap smear, and 24% had a family/friend history of cervical cancer. Eleven percent of women who vaccinated their children had a history of cervical cancer.

Odds ratios between sociodemographic and maternal experience variables on HPV vaccination uptake were calculated in separate logistic regression models. Table 1 shows that being between the ages of 11–13 (OR = 1.75, 95% CI = 1.36, 2.24) and a female child (OR = 1.31, 95% CI = 1.02, 1.70) predicted greater odd of HPV vaccination uptake among children. Personal history of abnormal Pap smear (OR = 1.50, CI = 1.15, 1.97), family/friend history of cervical cancer (OR = 1.72, CI = 1.26, 2.35), and personal history of cervical cancer (OR = 3.00, CI = 1.82, 4.95) predicted greater odds of HPV vaccine uptake in children. Additionally, perceived benefits were independently associated with greater odds of HPV vaccine uptake (OR = 2.78, CI = 2.34, 3.31).

Perceived benefits were examined as a mediator in three separate simple mediation analyses between maternal HPV experiences (individually) and HPV vaccination uptake while controlling for covariates. Perceived benefits mediated the relationship between history of abnormal Pap smear and HPV vaccination uptake (indirect effect = .146, SE = .069, 95% CI = .014, .289; see Figure 1). Additionally, perceived benefits mediated the relationship between family/friend history of cervical cancer and HPV vaccination uptake (indirect effect = .228, SE = .079, 95% CI = .080, .387; see Figure 2). Perceived benefits also served as a mediator between maternal history of cervical cancer and HPV vaccination uptake (indirect effect = .298, SE = .116, 95% CI = .082, .533; see Figure 3)

Figure 1. Perceived benefits mediates the relationship between history of abnormal Pap smear and HPV vaccination uptake

Figure 2. Perceived benefits mediates the relationship between family/friend history of cervical cancer and HPV vaccination uptake

Figure 3. Perceived benefits mediates the relationship between maternal history of cervical cancer and HPV vaccination uptake

Discussion

We found several important relationships between sociodemographics and maternal HPV experiences to HPV vaccine uptake in children. Children aged 11–13 y and female children had greater odds of vaccination uptake. Women who were younger and with maternal HPV experiences (including personal history of an abnormal Pap smear or cervical cancer and family/friend history of cervical cancer) had greater odds of initiating HPV vaccination for their children. The association between maternal HPV experiences and HPV vaccine uptake in children does appear to be at least partially explained by mothers’ perceived benefits of HPV vaccination because of significant indirect effects between each maternal experience and HPV vaccination uptake.

The current study extends previous literature by examining maternal HPV experiences on HPV vaccine uptake among both daughters and sons. Results are consistent with findings from several previous studies that have found that mothers’ history of STIs and abnormal Pap smears are associated with vaccine uptake among daughters.^6,7,18,19 Few studies, however, have examined the relationship between maternal HPV experiences and HPV vaccine uptake among both daughters and sons. One study found higher rates of HPV vaccination for sons among mothers with a history of genital warts, although this association did not reach statistical significance.²⁰ The current study adds to previous research by demonstrating that mothers’ history of abnormal Pap smears and a personal or family/friend history of cervical cancer is associated with HPV vaccination of both daughters and sons.

Little research has examined the association between maternal personal or family/friend history of cervical cancer on HPV vaccine uptake of children. In one study, mothers’ exposure to HPV-related disease (including history of cervical cancer and a friend or family member with cervical cancer) was not correlated with vaccine uptake among daughters,²¹ which is inconsistent with the findings of the current study. The current study, however, had a larger sample size of participants with a personal and family/friend history of cervical cancer, which could have increased power to detect a significant relationship.

The current study builds on existing literature showing that framing HPV vaccination as a disease-prevention tool may influence maternal vaccination decisions.²² Furthermore, clinicians and researchers may want to discuss HPV vaccination in the context of mothers’ personal narratives about HPV-related disease and cancers as a way of highlighting the potential adverse effects of non-vaccination. Recent intervention studies have found that personal narratives related to HPV vaccination are associated with positive attitudes toward vaccination,²³ increased knowledge of HPV,²³ and greater risk perception of HPV.²⁴ Furthermore, a review of narrative intervention studies concluded that narrative interventions appear to be promising strategies for promoting behavior change.²⁵ In the current study, the relationship between a friend/family member with cervical cancer and HPV vaccination uptake may have been influenced by personal narratives of cancer. Interestingly, personal narratives of female-affecting cancers could affect the vaccination of boys as well as girls, although further research examining this relationship is necessary.

We hypothesized that an explanation for the relationship between maternal HPV experiences and HPV vaccine uptake in children would be that women with a history of adverse experiences with HPV might see more benefits to HPV vaccination. Perceived benefits did help explain the relationship between women’s HPV experiences and HPV vaccination of children consistent with the HBM theoretical framework.¹¹ These results suggest that increasing perceived benefits to HPV vaccination in mothers with previous maternal HPV experiences will help increase vaccination uptake among children, which is similar to results from other studies that have shown perceived benefits to be related to intention to vaccinate²⁶ and vaccination uptake²⁷ in young adults. Along with personal narratives, interventionists may want to include messages related to the benefits of vaccination, such as safety of the vaccine and ability to prevent HPV-related disease, when promoting HPV vaccination of children.

Several limitations of this study must be noted. Participants were recruited nationally but were not a nationally representative sample. Vaccine uptake was measured by patient report rather than by medical record, limiting generalizability. The current study was limited to cervical cancer and no other HPV-related cancers such as oropharyngeal or anal, which could be a future area of research. Certain groups of women who are more likely to have a history of HPV-related disease, such as those with autoimmune disorders like Human Immunodeficiency Virus (HIV),²⁸ may even be more likely to vaccinate their children than women without this history; however, we did not measure whether women had these disorders. We asked for HPV vaccination information for the youngest child if a mother had more than one child, and HPV vaccination status and beliefs could differ between older and younger children. The current study targeted women who had a personal history of cervical cancer, which is more common in minority and low-socioeconomic status women,²⁹ who may have lower literacy levels and no access to the internet. Reports of cervical cancer in this study were higher than would be expected compared to prevalence rates of cervical cancer in the general population of US. Six percent of women in the sample reported a cervical cancer diagnosis yet the prevalence estimate in the United States is approximately 0.18%. Women may have confused high-grade, precancerous lesions with cancer or conflated cervical cancer with other gynecological cancers; or women with cervical cancer may have been more likely to respond to the survey. Perceived history of cervical cancer, however, is likely to be the most relevant factor related to vaccine uptake among children.

In conclusion, maternal HPV experiences, including personal history of an abnormal Pap smear, personal history of cervical cancer, and family/friend history of cervical cancer, are all associated with HPV vaccine uptake among children. Perceived benefits of HPV vaccination helped explain the relationship between maternal HPV experiences and HPV vaccination uptake. Further research should include women with other HPV-related cancers and autoimmune disorders to determine if other adverse HPV experiences are related to vaccination uptake. The results from the current study suggest that clinicians and interventionists may consider the use of mothers’ personal narratives and perceived benefits to frame HPV vaccination messaging.

Additional information

Funding

Research reported in this publication was supported in part by the Center for HPV Research, which is funded by the Indiana University–Purdue University Indianapolis Signature Centers Initiative in conjunction with the Indiana University School of Medicine Department of Pediatrics and the Indiana University Melvin and Bren Simon Cancer Center. The research also was supported by the National Cancer Institute of the National Institutes of Health under Award Number T32CA117865 and the National Institute of Nursing Research of the National Institutes of Health under Award Number F31NR018791. Its content is solely the responsibility of the authors and does not necessarily represent the official views of Indiana University or the National Institutes of Health, including the National Cancer Institute and National Institute of Nursing Research.