Relationship between maternal experiences and adolescent HPV vaccination

ABSTRACT

The human papillomavirus (HPV) vaccine has been available for over a decade but its uptake rate is still low. To explore the relationship between the HPV vaccination status of a child and their mother's beliefs, behaviors and knowledge, we surveyed 1497 women with at least one child aged 9–17 y between September 2011 and November 2015. Physician recommendation was the most important factor associated with reported child vaccination status. Mothers who reported receiving a provider recommendation for the HPV vaccine were 32 times more likely to have a child who had been vaccinated compared with mothers who did not report provider recommendation (aOR) = 32.17; 95% CI: 21.77, 47.54). Knowing someone who had received the vaccine was also strongly associated with vaccination uptake (59% vs 12%, p < .001). Additionally, prior HPV diagnosis (aOR = 1.91; 95% CI: 1.18, 3.10) and knowing someone with cervical cancer (aOR = 1.38; 95% CI: 1.01, 1.89) were associated with child vaccination status. Mothers who perceived moderate to high risk for their child contracting HPV or developing genital warts or cervical cancer were more likely to report that their daughters (but not their sons) had been vaccinated.

Although the human papillomavirus (HPV) vaccine has been available for over a decade, its uptake rate is still low.¹ The CDC estimates that around 60% of adolescent girls 13–17 y of age had initiated the vaccine series as of 2015. Initiation rates for boys are even lower (50%).¹

To help determine how these rates could be improved, studies have examined factors associated with HPV vaccination. For example, provider recommendation, parental knowledge, and insurance are associated with vaccination. Parents often believe that their children are not likely to get an HPV infection, but the relationship between this belief and vaccination status is unknown.^2,3 Moreover, little is known about how different sources of information on the HPV vaccine influence initiation of the series.^4-7 The purpose of this study was to address these gaps in the literature to improve efforts to develop future interventions.

Women with at least one child 9–17 y of age presenting for care at a reproductive health clinic in southeast Texas between September 2011 and November 2015 were invited to participate in a self-administered questionnaire about HPV vaccination. Overall, 1509 women who met the eligibility criteria were asked to participate. Twelve declined, leaving 1497 women. All participants consented to the study and received $5 for their participation. This study was approved by The University of Texas Medical Branch Institutional Review Board.

The questionnaire, which was available in English or Spanish, asked about demographic information and medical history (self-reported prior mammograms, prior diagnosis of HPV infection, cervical dysplasia or cervical cancer). The questionnaire was not validated. The specific language on the questionnaire regarding prior HPV infection was: “Have you ever been diagnosed with the human papillomavirus (HPV) infection?” The specific language regarding healthcare provider recommendation was: “Has your health care provider ever recommended that your daughter get Gardasil?” Response options for both of these questions were “Yes” and “No.” Questions about exposure to HPV-related information asked about sources of information, if the participant had acquaintance(s) who had received the HPV vaccine, and if women knew someone who had experienced side effects from the vaccine. Additional questions included whether the participant knew someone who had cervical cancer and whether their child's provider had recommended the HPV vaccine. Mothers rated their children's risk of contracting HPV, developing genital warts or developing cervical cancer in the absence of HPV vaccination on a scale of 0% to 100%. Perceived risks were categorized into 3 groups (high (≥ 70%), medium (≥ 30 to <70%), and low (< 30%)) based on the score.

Children who had received ≥ 1 dose of the HPV vaccine were categorized as initiators (vaccinated). Those who had not received any doses were categorized as non-initiators (unvaccinated). Vaccination status was coded as a binary variable.

In this cross-sectional study design, chi-square tests were used to examine differences in reported child vaccination status by maternal characteristics and experiences. Multivariable logistic regression models assessed the association of maternal experiences and perceived risk with child vaccination status. The year the survey was administered, child's sex, maternal age, race, and income were all adjusted for in final models. Data were analyzed using SAS® software 9.4 (Cary, North Carolina).

Among 1497 participants, 17% (n = 256) had at least one daughter or son who had initiated the HPV vaccine series. HPV vaccination rates in this region of Texas are even lower than they are nationally: in our population, 20% of girls and only 11% of boys had received at least one dose of the HPV vaccine. Children's vaccination status did not vary by maternal history of cervical dysplasia or by whether they knew someone who had experienced a negative side effect from the vaccine. Significant differences were observed between mothers with vaccinated compared with unvaccinated children regarding mothers' self-report of a prior diagnosis of HPV(11% vs 7%, p = .01), mammography status (40% vs 33%, p = .04), whether a provider had ever recommended the vaccine (79% vs 10%, p < .001), if they knew someone with cervical cancer (38% vs 32%, p = .05), had learned about HPV from a health education class (21% vs 14%, p = .01), knew someone who had received the HPV vaccine (59% vs 12%, p < .001), or had seen an advertisement about the vaccine (74% vs 51%, p < .001) (Table 1).

Table 1.

Vaccination status of child by mother's experience among women attending reproductive clinic in Texas (N = 1497).

Characteristics	All groups (N = 1497), n (%)	Unvaccinated (n = 1241), n (%)	Vaccinated (n = 256), n (%)	P-value*
Race/Ethnicity				0.006
Non-Hispanic Black	454 (30.7)	361 (79.5)	93 (20.5)
Non-Hispanic White	265 (17.9)	212 (80)	53 (20)
Hispanic	760 (51.4)	653 (85.9)	107 (14.1)
Missing = 18
Age				0.0001
20–29	221 (14.8)	205 (92.8)	16 (7.2)
30–39	885 (59.1)	723 (81.7)	162 (18.3)
40+	391 (26.1)	313 (80)	78 (20)
History of HPV infection				0.01
Yes	111 (7.44)	82 (73.87)	29 (26.13)
No	1381 (92.50)	1155 (83.64)	226 (16.36)
Missing = 5
History of abnormal pap smear test/atypical, precancerous cervical cells, or cervical cancer				0.41
Yes	1045 (69.90)	873 (83.54)	172 (16.46)
No	450 (30.10)	368 (81.78)	82 (18.22)
Missing = 2
Prior mammogram				0.04
Yes	512 (34.41)	410 (80.08)	102 (19.92)
No	976 (65.59)	823 (84.32)	153 (15.68)
Missing = 9
Prior STD test				0.04
Yes	821 (54.99)	666 (81.12)	155 (18.88)
No	672 (45.01)	572 (85.12)	100 (14.88)
Missing = 4
Recommendation by health provider				<0.001
Yes	330 (22.10)	127 (38.48)	203 (61.52)
No	1163 (77.90)	1110 (95.44)	53 (4.56)
Missing = 4
Characteristics	All groups, N = 1497 (%)	Unvaccinated, n = 1241 (%)	Vaccinated, n = 256 (%)	P-value *
Knows woman with cervical cancer				0.05
Yes	493 (32.95)	395 (80.12)	98 (19.88)
No	1003 (67.05)	845 (84.25)	158 (15.75)
Missing = 1
Heard HPV information from health education class				0.01
Yes	227 (15.20)	174 (76.65)	53 (23.35)
No	1266 (84.80)	1063 (83.97)	203 (16.03)
Missing = 4
Knows anyone who had side effects from a vaccine				0.12
Yes	86 (5.77)	66 (76.74)	20 (23.26)
No	1404 (94.23)	1168 (83.19)	236 (16.81)
Missing = 7
Knows anyone who had received HPV vaccine				<0.001
Yes	298 (20.14)	149 (50.00)	149 (50.00)
No	1182 (79.86)	1077 (91.12)	105 (8.88)
Missing = 17
Has seen ad on TV, a magazine, or brochure about HPV				<0.001
Yes	816 (54.55)	628 (76.96)	188 (23.04)
No	680 (45.45)	613 (90.15)	67 (9.85)
Missing = 1

^*P-value was obtained by using 2-sided and only no-missing observations for comparing unvaccinated and vaccinated groups.

Results from multivariable regression models demonstrated that the strongest association with vaccination was having received a vaccine recommendation from their child's health care provider (adjusted odds ratio (aOR = 32.17; 95% CI: 21.77, 47.54). Furthermore, mothers were >10 times more likely to vaccinate their child if they knew someone who had been vaccinated against HPV compared with those who did not (aOR = 10.24; 95% CI: 7.35, 14.27). Women who reported prior HPV infection were almost twice as likely to report their child had initiated the vaccine series compared with mothers who did not report prior HPV infection (aOR = 1.91; 95% CI: 1.18,3.10). Moreover, women who knew someone with a history of cervical cancer were 38% more likely to report that their child was vaccinated (aOR = 1.38; 95% CI: 1.01,1.89). Mothers who had received information from a health education class (aOR = 1.48; 95% CI: 1.02, 2.14) or seen an advertisement about the HPV vaccine or read a brochure about HPV (aOR = 2.92; 95% CI: 2.09, 4.08) were also more likely to report their child had initiated HPV vaccination.

Mothers who perceived that their daughters were at high risk of acquiring HPV or developing genital warts were more likely to have had them vaccinated compared with mothers who perceived that their daughter's risk was low (Table 2). In contrast, mothers who believed that their sons' risk of acquiring HPV or developing genital warts was high were not more likely to get them vaccinated (aOR: 1.85; 95% CI: 0.77, 4.46). Finally, mothers who rated their daughters' chance of getting cervical cancer as high were more likely to have reported that their daughters were vaccinated compared with those who perceived their daughter's risk of cervical cancer to be low.

Table 2.

Assessment of perceived risk and effect on HPV vaccine uptake (N = 1497).

	Model 1a (n = 947)		Model 2b (n = 922)
Perceived risk of outcome without HPV vaccination	Frequency (%)	aORc (95% CI)	Frequency (%)	aORc (95% CI)
Chance to contract HPV
High*	180 (19.46)	2.69 (1.55 – 4.68)	148 (16.52)	1.50 (0.61 – 3.66)
Medium**	321 (34.70)	1.93 (1.17 – 3.19)	311 (34.71)	1.65 (0.78 – 3.47)
Low***	424 (45.84)	Reference	437 (48.77)	Reference
Chance to develop genital warts
High*	161 (17.46)	2.79 (1.61 – 4.84)	140 (15.64)	1.85 (0.77 – 4.46)
Medium**	293 (31.78)	2.05 (1.25 – 3.34)	299 (33.41)	1.77 (0.83 – 3.78)
Low***	468 (50.76)	Reference	456 (50.95)	Reference
Chance to develop cervical cancer		Only daughter
High*	173 (18.70)	3.17 (1.83 – 5.50)
Medium**	303 (32.76)	1.88 (1.15–3.09)
Low***	449 (48.54)	Reference
HPV could harm future health of child
Agree	522 (72.70)	0.58 (0.36, 0.92)	552 (74.20)	1.12 (0.63, 2.00)
Neutral	84 (11.70)	0.35 (0.17, 0.72)	80 (10.75)	0.52 (0.22, 1.25)
Disagree	112 (15.60)	Reference	112 (15.05)	Reference
HPV could harm future relationship	496 (69.56)	0.70 (0.45, 1.09)	539 (73.04)	1.07 (0.60, 1.89)
Agree	78 (10.94)	0.29 (0.13, 0.63)	79 (10.70)	0.45 (0.18, 1.09)
Neutral
Disagree	139 (19.50)	Reference	120 (16.26)	Reference
Would be devastated if child got HPV
Agree	665 (71.89)	0.57 (0.38, 0.87)	676 (74.04)	0.55 (0.34, 0.89)
Neutral	113 (12.22)	0.59 (0.32, 1.07)	100 (10.95)	0.37 (0.18, 0.78)
Disagree	147 (15.89)	Reference	137 (15.01)	Reference
HPV could hinder her ability to become pregnant in the future		Only daughter
Agree	418 (66.03)	0.68 (0.43, 1.08)
Neutral	85 (13.43)	0.37 (0.18, 0.74)
Disagree	130 (20.54)	Reference

^aIncluded women who has at least one daughter

^bIncluded women who has at least one son

^cAdjusted for time, mother's age, any daughter, race, and income

^*Perceived risk ranging from 70–100%

^**Perceived risk ranging from 30–60%

^***Perceived risk ranging from 0–20%

Abbreviations: aOR = adjusted odds ratio; 95% CI = 95% confidence interval

This study found that maternal exposure to different sources of information had a significant effect on HPV vaccine uptake. However, not all sources of information were equally effective. Provider recommendation was most strongly associated with reported child vaccination status: mothers who reported provider recommendation for the HPV vaccine were 32 times more likely to have a child who had been vaccinated. This finding aligns with previous reports that provider recommendation is strongly associated with vaccination.^4-8 It is possible that some participants' reports of provider recommendation were based on the provider responding to the participants' question. In other words, without prompting from the provider, a parent may ask about the need for the vaccine and consider a positive response to be a recommendation. This is a significantly different situation than parents who receive a provider-initiated recommendation. Nonetheless, the high odds ratio we detected using data collected through 2015 demonstrates that provider recommendation continues to be extremely important to HPV uptake. This underscores the need to develop and disseminate more interventions to help improve provider recommendation to all eligible patients. These interventions should also address provider barriers. For example, discomfort with discussing sexuality before recommending the vaccine and lack of adequate reimbursement are barriers cited by physicians that should be addressed.⁹ One potential method for reducing provider barriers has been presented by the CDC, which now suggests that providers normalize the vaccine by offering it as part of the standard adolescent immunization package.¹⁰ In the model script, the issue of sexuality is not addressed.

Knowing someone who had received the vaccine was also strongly associated with having a child who had initiated the HPV vaccine. This is consistent with a study which demonstrated that HPV vaccination rates have a strong geographic dependence, indicating that communities where people know others who vaccinated their children may have a higher uptake.¹¹ We cannot determine if this association was causal as it is possible that mothers who believed in vaccinating their children spoke primarily with like-minded persons. However, it is also possible that knowing individuals who were vaccinated and did not experience serious side effects may have made the mother believe that the practice was safe and acceptable, as concerns about side effects are also a well-known barrier. If this is true, then educational efforts led by peers may be effective.

We also found a modest effect of HPV vaccine advertisements and information from their child's school on vaccine uptake. Thus, magazine and television ads appear to contribute to willingness to vaccinate. Taken together, these findings support the dissemination of information from numerous sources and individuals in both verbal and written format to increase vaccination rates in the US.

Overall, the mothers' health behaviors and experiences had little impact on whether she vaccinated her child. The 2 exceptions to this were whether she reported previously being diagnosed with HPV and if she knew someone with cervical cancer. The most likely explanation for this is that these women were more aware of HPV and its consequences than other parents. This suggests that it may be effective to discuss HPV vaccination at gynecologic visits with mothers of adolescent children, especially if the mother has been previously diagnosed with HPV or had an abnormal Pap smear.

Mothers who perceived their child's risk of contracting HPV or developing genital warts or cervical cancer to be moderate to high were more likely to vaccinate their daughters, but not their sons. Thus, educating women about the risk of their child contracting HPV currently may be more effective among mothers with daughters. However, mothers of sons also need to be educated that boys are at risk. A recent national study showed that 45% of US males ages 18–59 y are positive for HPV and 25% are positive for a high-risk strain.¹² Only 11% of eligible men were vaccinated against HPV.

This study has several limitations. All data, including child vaccination status and maternal history of HPV infection, were collected by self-report and were not verified by medical records. We cannot determine causality due to the cross-sectional nature of the study. The survey asked mothers if a health care provider recommended the HPV vaccine for their children. However, it did not distinguish if the mother asked about the vaccine first or if the health care provider initiated the HPV-vaccine discussion. Thus, there is the possibility of some confounding in the relationship between provider recommendation and HPV vaccine uptake. In addition, this survey was conducted in one geographical area and may not be generalizable to the rest of the US.

In conclusion, we found that mothers who had been exposed to information on the HPV vaccine, regardless of the source, were more likely to have vaccinated their child. Physician recommendation is one of the most important factors followed by exposure to others who have been vaccinated. These findings support that educating providers and patients is key to improving HPV vaccination rates in the US.

Abbreviation

HPV

Human papillomavirus

Disclosure of potential conflicts of interest

The authors report no conflict of interest.

Acknowledgment

The authors thank Keitha Moseley-Dendy, MA of UTMB for her assistance with manuscript preparation.

Funding

Dr. Fuchs is supported by an institutional research career development award (K12HD052023: Building Interdisciplinary Research Careers in Women's Health Program-BIRCWH; Berenson, PI) from the Office of Research on Women's Health (ORWH) and the Eunice Kennedy Shriver National Institute of Child Health and Human Development (NICHD) at the National Institutes of Health (NIH). Dr. Fuchs and Dr. Brown worked on the project as postdoctoral fellows supported by an institutional training grant (National Research Service Award T32HD055163, Berenson, PI) from NIH/NICHD.