Abstract
Introduction:
Parent and child vaccination behavior is related for human papillomavirus (HPV) and flu vaccine. Thus, it is likely that parental vaccination status is also associated with their children’s adherence to guideline-concordant childhood vaccination schedules. We hypothesized that parent influenza (flu) vaccination would be associated with their child’s vaccination status at age two.
Methods:
We used electronic health record data to identify children and linked parents seen in a community health center (CHC) within the OCHIN network (292 CHCs in 16 states). We randomly selected a child aged <2 years with ≥1 ambulatory visit between 2009-2018.
Employing a retrospective, cohort study design, we used general estimating equations logistic regression to estimate the odds of a child being up-to-date on vaccinations based on their linked parents’ flu vaccination status. We adjusted for relevant parent and child covariates and stratified by mother only, father only, and two-parent samples.
Results:
The study included 40,007 family-units: mother only = 35,444, father only = 2,784, and two parents = 1,779. A higher percentage of children were fully vaccinated if their parent or parents received a flu vaccine. Children in the two-parent sample whose parents both received a flu vaccine had more than twice the odds of being fully vaccinated, and two and a half times the odds of being fully vaccinated except flu vaccine compared to children with two parents who did not receive a flu vaccine (covariate-adjusted odds ratio [aOR] = 2.39, 95% CI = 1.67, 3.43 and aOR = 2.54, 95% CI = 1.54, 4.19, respectively).
Conclusions:
Parent flu vaccination is associated with routine child vaccination. Future research is needed to understand if this relationship persists over time and in different settings.
Keywords: Family health, Child health, Health service research, Childhood vaccination
1. Introduction
To prevent infectious and communicable diseases, the Center for Disease Control (CDC) recommends routine vaccination schedules for children and adolescents [1]. These routine vaccinations for children under the age of two include: Diphtheria, Tetanus, acellular Pertussis (DTaP); Polio; Measles, Mumps, Rubella (MMR); Haemophilus influenza type b (HIB); Hepatitis B (Hep B); Varicella; Pneumococcal; Hepatitis A (Hep A); Influenza (flu); and Rotavirus [1,2]. Flu vaccination recommendations for this age group began in 2004, as the Advisory Committee on Immunization Practices found the risks for morbidity and mortality for young children were higher than among older children and younger adults [3-5]. Overall, vaccination rates for U.S. children are >90% [6], however, few children receive all vaccines exactly as recommended [7-9] and those without health insurance coverage or with Medicaid coverage have lower rates than those with private health insurance [10]. For example, in 2019, 57.9% of children with commercial health management organization (HMO) insurance were up to date with all vaccinations recommended by the age of two, whereas only 38.1% of children with Medicaid HMO insurance were up to date [8]. Unvaccinated children risk the recurrence of many preventable diseases that were once considered eradicated. For example, despite being declared ‘eliminated,’ the CDC reported 704 cases of measles in 2019: the majority of which occurred in under-immunized communites [11].
Several factors are associated with increased childhood vaccination rates, including school mandates [12], enrollment in the Women, Infants, and Children public assistance program, white race, college education [9,13,14], private health insurance [13], and lack of poverty [15]. Parent attitudes and beliefs also impact vaccination rates [16]. For example, parents who believed the flu vaccine reduced risk, duration, and severity of the flu, were more likely to vaccinate their children for the flu than parents that did not believe those things [17].
Since vaccination of a child is dependent on parent decision-making and vaccine hesitant parents are less likely to vaccinate their children [18,19], it is likely that parent and child vaccination behavior is related. Indeed, one study found that mothers who received human papillomavirus (HPV) vaccine were 3.5 times more likely to report HPV vaccination for their children than unvaccinated mothers [20] and survey research found parents who received the flu vaccine were more likely to report vaccinating their children for the flu [17,21]. Thus, it is likely that parental flu vaccination status is also associated with their children’s adherence to guideline-concordant childhood vaccination schedules beyond just the flu vaccine. Understanding parental vaccination impact on their children’s status may help devise interventions to increase vaccination coverage among children. Therefore, the goal of this study was to estimate the association of parental flu vaccine status on whether a child is fully vaccinated by age two among a cohort of linked parents and children who were patients seen in community health centers (CHCs) [22]. As CHCs see 1 in 8 children in the U.S. and care for patients regardless of health insurance status or ability to pay, the majority of CHC patients are uninsured or Medicaid insured and have low-incomes [23]. Since children with Medicaid coverage or who are uninsured and those living in poverty have lower vaccination rates than privately insured and children not living in poverty [13,15,24], identifying any additional factors associated with vaccine receipt could help increase rates in this population. We hypothesized that children of parents who received the flu vaccine would have greater compliance for guideline-concordant childhood vaccination schedules than parents without the flu vaccine.
2. Methods
2.1. Data source
We identified linked family-units in a network of CHCs consisting of a single instance of Epic© electronic health record (EHR) using a previously validated algorithm [22,25]. These units consisted of children aged 0–17 and linked parent(s) using emergency contacts or account guarantor fields indicating that the relationship was ‘mother’ or ‘father.’ We then connected the linked parent and child dataset to EHR data from the Accelerating Data Value Across a National Community Health Center (ADVANCE) clinical research network (CRN) of PCORnet® [26]. We included CHCs that provided healthcare to parents and children from 2009 to 2018. For this analysis, we selected children between the ages of 12–24 months to focus on recommended childhood immunizations during this time period.
2.2. Population
We identified 55,748 distinct children having at least one ambulatory visit between the ages of 12–24 months from 292 CHCs in 16 states during the 2009–2018 study period. These children belonged to 40,007 family-units. We randomly selected one child from each family-unit for this study, as the high intraclass correlation of vaccinations among siblings within a family would produce unstable models. As we suspected potential heterogeneity in association, we identified three mutually exclusive samples of family-units in which the child was linked to: 1) ‘mothers only’ (n = 35,444); 2) ‘fathers only’ (n = 2,784); and, 3) ‘two parents’ (n = 1,779). For the two-parent sample, we included 173 where both parents were the same sex.
2.3. Dependent variables
The outcome measures were binary indicators for the child having all recommended vaccinations or all recommended vaccinations minus flu as of the date prior to their second birthday. All recommended vaccinations were identified using the combination of Current Procedural Terminology (CPT) and Codes for Vaccine Administered (CVX) and included the following with number of doses in parentheses: DTaP (4); Polio (3); MMR (1); Hib (3); Hep B (3); Varicella (1); Pneumococcal (4); Hep A (1); Flu (2); and Rotavirus (≥2) [1,14]. Of note, novel influenza-H1N1-09 vaccines were excluded from the flu count, as this was a second flu vaccine administered during only one year. We combined these into two measures of vaccination status for the children per the Core Set of Children’s Health Care Quality Measures for Medicaid and the Children’s Health Insurance Program technical specifications [2]. The first measure we assessed was ‘combination 10′, which included all vaccinations listed above [14]. Since previous research showed flu vaccine for children by age two is particularly low [27,28], we also included a second outcome that combined all vaccines except for flu (known as ‘combination 7′ in the Core Set of Children’s Health Care Quality Measures) [2].
2.4. Independent variables
The main independent variable for the mother only and father only groups was a binary variable denoting whether or not the parent received at least one flu vaccination prior to their child’s second birthday, including 10 months prior to the child’s birthdate. Parent flu vaccine was defined using the combination of CPT and CVX codes, again excluding H1N1 vaccines. If a child linked to two parents, we included a set of indicator variables that distinguished whether neither, one, or both parents received at least one flu vaccine during the observation period.
2.5. Covariates
Based on previous research indicating factors associated with vaccination status [13-15], we adjusted the mother and father only samples for the following child covariates: child’s last known insurance status prior to age two (private insurance, public insurance, uninsured), number of chronic conditions listed in the patient’s problem list unresolved by child’s second birthday, U.S. region (Northeast, South, Midwest, West). We also adjusted for the following parent covariates: parent age at child’s second birthday, race and ethnicity (non-Hispanic white, non-Hispanic Black, non-Hispanic other, Hispanic, not recorded), preferred language (English, non-English), last recorded federal poverty level (FPL) at visit categorized as (>138%, ≤138%, not recorded), last known health insurance status (private insurance, public insurance, uninsured), number of ambulatory visits in the child’s first two years of life, and number of unresolved chronic conditions documented in the patient’s problem list as of child’s second birthday. Visit and chronic condition categories for parent and child were based on their distributions.
For the analyses of children linked to two parents, we again adjusted for child’s insurance status, unresolved chronic conditions, and U.S. region and each parent’s age, number of visits, and unresolved chronic conditions; further, we aggregated parent data for race and ethnicity using the same values as before if parents identified equivalently or used the value different race and ethnicity if parent-reported values did not agree; we used an indicator for if at least one parent preferred English language; insurance status and FPL combined each parent’s individual value as described above.
2.6. Statistical analysis
For each parent group, we described characteristics overall and by whether or not the parent had at least one flu vaccine. Next, we graphically display the unadjusted percent of children up to date with vaccinations by age two years, each calendar year for children linked to mothers only, fathers only, and both parents based on parent flu vaccine status. We graph this for both the fully vaccinated and the fully vaccinated minus flu outcomes. We then used general estimating equations (GEE) logistic regression to estimate the odds of a child being up to date on all recommended vaccinations and all minus flu prior to their second birthday, for each of the three samples adjusted for all covariates. Collinearity was assessed by variance inflation factor estimation and was not found to be an issue. A robust sandwich variance estimator with an exchangeable correlation structure was used in all models to account for clustering on the child’s primary CHC. We performed sensitivity analyses to assess the influence of both parent and child clinic utilization separately by stratifying on the number of visits during the study period. GEE-derived adjusted odds ratios (aOR) and 95% confidence intervals (CI) were estimated and reported. All analyses utilized two-sided testing with set 5% type I error and were conducted using Stata 15.
This study was approved by the Oregon Health and Science University Institutional Review Board [ID#: STUDY00019958].
3. Results
The final total number of family-units was 40,007: the mother only sample included 35,444, the father only sample included 2,784, and our two-parent sample included 1,779. We report characteristics of the mother only sample in Table 1 and the father only and two parents’ groups in Appendix Tables A1-A2. Focusing on the mother only sample, the median age of mothers was 29. Over half were Hispanic (51.1%) and the majority had public health insurance (64.8%). Most mothers did not have any unresolved chronic conditions (52.3%) and two or more visits (77%). Of the linked children, 87.3% had public health insurance, 67.3% had family incomes ≤ 138% FPL, and 61.0% had nine or more visits during the study period (Table 1).
Table 1.
Characteristics of mother-only sample, child having had at least one ambulatory visit between the ages of 12 – 24 months (2009–2018).
| Group, No. (%) | |||
|---|---|---|---|
| Parent Had >=1 Flu Vaccine During Study Period | |||
| Parent Characteristics | All | No | Yes |
| N = 35444 | N = 17354 | N = 18090 | |
| Age at Child’s Second Birthday | median = 29, range:14–57 | median = 28, range:14–57 | median = 29, range:14–57 |
| Race and Ethnicity | |||
| Hispanic | 18,111 (51.1%) | 7607 (43.8%) | 10,504 (58.1%) |
| Non-Hispanic White | 10,057 (28.4%) | 6070 (35.0%) | 3987 (22.0%) |
| Non-Hispanic Black | 4355 (12.3%) | 2261 (13.0%) | 2094 (11.6%) |
| Non-Hispanic Other | 1679 (4.7%) | 700 (4.0%) | 979 (5.4%) |
| Unknown | 1242 (3.5%) | 716 (4.1%) | 526 (2.9%) |
| English Language Preferred | 20,769 (58.6%) | 11,658 (67.2%) | 9111 (50.4%) |
| Last Known Insurance Status | |||
| Private | 4093 (11.5%) | 2117 (12.2%) | 1976 (10.9%) |
| Public | 22,960 (64.8%) | 11,389 (65.6%) | 11,571 (64.0%) |
| Uninsured | 8391 (23.7%) | 3848 (22.2%) | 4543 (25.1%) |
| Unresolved Chronic Conditions a | |||
| 0 | 18,728 (52.8%) | 10,478 (60.4%) | 8250 (45.6%) |
| 1 | 8059 (22.7%) | 3377 (19.5%) | 4682 (25.9%) |
| >1 | 8657 (24.4%) | 3499 (20.2%) | 5158 (28.5%) |
| Visits During Study | |||
| 0 | 4361 (12.3%) | 3630 (20.9%) | 731 (4.0%) |
| 1 | 3795 (10.7%) | 2573 (14.8%) | 1222 (6.8%) |
| 2–4 | 9725 (27.4%) | 5150 (29.7%) | 4575 (25.3%) |
| 5+ | 17,563 (49.6%) | 6001 (34.6%) | 11,562 (63.9%) |
| Child Characteristics | |||
| Female | 17,382 (49.0%) | 8438 (48.6%) | 8944 (49.4%) |
| Last Known Insurance Status | |||
| Private | 2573 (7.3%) | 1422 (8.2%) | 1151 (6.4%) |
| Public | 30,938 (87.3%) | 14,839 (85.5%) | 16,099 (89.0%) |
| Uninsured | 1933 (5.5%) | 1093 (6.3%) | 840 (4.6%) |
| Last Known Federal Poverty Level | |||
| <=138% | 23,868 (67.3%) | 11,534 (66.5%) | 12,334 (68.2%) |
| >138% | 4586 (12.9%) | 2287 (13.2%) | 2299 (12.7%) |
| Not Documented | 6990 (19.7%) | 3533 (20.4%) | 3457 (19.1%) |
| Unresolved Chronic Conditions a | |||
| 0 | 29,059 (82.0%) | 14,567 (83.9%) | 14,492 (80.1%) |
| 1+ | 6385 (18.0%) | 2787 (16.1%) | 3598 (19.9%) |
| Visits During Study | |||
| 1 | 2529 (7.1%) | 1866 (10.8%) | 663 (3.7%) |
| 2–3 | 3299 (9.3%) | 2283 (13.2%) | 1016 (5.6%) |
| 4–8 | 7993 (22.6%) | 4629 (26.7%) | 3364 (18.6%) |
| 9+ | 21,623 (61.0%) | 8576 (49.4%) | 13,047 (72.1%) |
| Region b | |||
| Northeast | 2846 (8.0%) | 860 (5.0%) | 1986 (11.0%) |
| South | 488 (1.4%) | 365 (2.1%) | 123 (0.7%) |
| Midwest | 4344 (12.3%) | 2182 (12.6%) | 2162 (12.0%) |
| West | 27,766 (78.3%) | 13,947 (80.4%) | 13,819 (76.4%) |
Flu = influenza vaccine (excludes H1N1).
Note = characteristics for the fathers only and two parents are in Appendix Tables 1-2.
The number of chronic conditions listed in the patient’s problem list that are unresolved as of study end.
States include: Northeast (MA); South (FL, GA, NC, TX); Midwest (IN, MN, OH, WI); West (AK, CA, MT, NV, OR, UT, WA).
Unadjusted percentages for children age two or less being fully vaccinated ranges from 14.4% in 2009 in the mothers only sample to 28.9% in the two parents’ sample in 2018. Whereas the percentages for children being fully vaccinated except flu, vaccine ranges from 29.4% in 2009 in the father only sample to 65.6% in the mother only sample in 2016. Child vaccination rates are shown in Appendix Table A3. Parent flu vaccine ranges from a low of 6.3% for both parents in the two-parent sample in 2010 to a high of 58.6% in the mother only sample in 2018 (Table 2). Overall, both flu vaccination for parents and child vaccination rates increased from 2009 to 2018.
Table 2.
Unadjusted prevalence of parent vaccination status by year child turned age two years by parent sample.
| Flu Vaccination, % | ||||
|---|---|---|---|---|
| Mother only | Father only | Two-parent Sample | ||
| Yeara | Parent flu | Parent flu | 1 Parent flu | 2 Parents flu |
| 2009 | 32.9 | 11.8 | 35.6 | 11.1 |
| 2010 | 33.5 | 14.9 | 38.3 | 6.3 |
| 2011 | 37.2 | 19.6 | 37.4 | 18.7 |
| 2012 | 43.2 | 21.5 | 39.2 | 13.3 |
| 2013 | 49.7 | 28.6 | 33.0 | 19.9 |
| 2014 | 52.0 | 28.5 | 39.2 | 29.2 |
| 2015 | 53.3 | 32.9 | 44.9 | 27.8 |
| 2016 | 56.1 | 34.7 | 37.9 | 31.6 |
| 2017 | 56.0 | 43.9 | 30.7 | 39.8 |
| 2018 | 58.6 | 44.9 | 39.4 | 37.0 |
Flu = influenza vaccine.
Prevalence shown for parents is of having received a flu vaccine during the child’s first two years of life including gestation period.
Visit and chronic condition categories for parent and child were based on their distributions.
Year the child turned two years old.
In all three samples, a higher percentage of children were fully vaccinated if their parent or parents received a flu vaccine with higher percentages in the mother only compared to the father only samples. Patterns were similar for both fully vaccinated and fully vaccinated except flu (Figs. 1 and 2).
Fig. 1. a-c: Unadjusted prevalence of fully vaccinated children (combination 10) by age two by parent sample.
Combination 10 vaccination (number required): Diphtheria, Tetanus, acellular Pertussis (4); Polio (3); Measles, Mumps, Rubella (1); Haemophilus influenza type b (3); Hepatitis B (3); Varicella; Pneumococcal; Hepatitis A (1); Influenza (2); Rotavirus (≥2). [1,2].
Fig. 2. a-c. Unadjusted prevalence of fully vaccinated children (combination 7) by age two by parent sample.
Combination 7 vaccination (number required): Diphtheria, Tetanus, acellular Pertussis (4); Polio (3); Measles, Mumps, Rubella (1); Haemophilus influenza type b (3); Hepatitis B (3); Varicella; Pneumococcal; Hepatitis A (1); Rotavirus (≥2). [1,2].
Children in the mother only sample had twice the odds of being fully vaccinated (combination 10) if their mother received a flu vaccine in comparison to children whose mother did not receive a flu vaccine (covariate-adjusted odds ratio [aOR] = 2.03, 95% CI = 1.80, 2.29). Children in the father only sample had 1.70 times the odds if their father received a flu vaccine in comparison to children whose father did not receive a flu vaccine (aOR = 1.70, 95% CI = 1.37, 2.11). In the two-parent sample, children of parents who both received a flu vaccine had more than twice the odds of being fully vaccinated compared to children with two parents who did not receive a flu vaccine (aOR = 2.39, 95% CI = 1.67, 3.43).
Children in the mother only sample had 1.53 times the odds of being fully vaccinated except flu vaccine (combination 7) if their mother received a flu vaccine in comparison to children whose mother did not receive a flu vaccine (aOR = 1.53, 95% CI = 1.39, 1.69). The effect size observed in the father only sample was (aOR = 1.19, 95% CI = 1.003, 1.41). In the two-parent sample, children of parents who both received a flu vaccine had two and a half times the odds of being fully vaccinated compared to children with two parents who did not receive a flu vaccine (aOR = 2.54, 95% CI = 1.54, 4.19) (Table 3).
Table 3.
Association between parents’ flu vaccine status and child being fully vaccinated by age two.
|
Child Fully Vaccinated
(Combination 10) |
Child Fully Vaccinated Except Flu (Combination 7) | |||
|---|---|---|---|---|
|
|
|
|||
| Influenza Vaccine Receipt | Unadjusted Odds Ratio (95% CI) | Adjusted Odds Ratio (95% CI) |
Unadjusted Odds Ratio (95% CI) |
Adjusted Odds Ratio (95% CI) |
| Mother only sample | ||||
| Mother received vaccine | 2.36 (2.09, 2.67) | 2.03 (1.80, 2.29) | 1.74 (1.58, 1.90) | 1.53 (1.39, 1.69) |
| Father only sample | ||||
| Father received vaccine | 1.75 (1.46, 2.09) | 1.70 (1.37, 2.11) | 1.20 (1.04, 1.39) | 1.19 (1.00, 1.41) |
| Two parent sample | ||||
| One parent received vaccine | 2.27 (1.68, 3.06) | 1.92 (1.42, 2.60) | 2.20 (1.50, 3.21) | 1.88 (1.25, 2.83) |
| Both parents received vaccine | 2.69 (2.00, 3.62) | 2.39 (1.67, 3.43) | 2.39 (1.60, 3.57) | 2.54 (1.54, 4.19) |
Flu = influenza vaccine.
Combination 10 vaccination (number required): Diphtheria, Tetanus, acellular Pertussis (4); Polio (3); Measles, Mumps, Rubella (1); Haemophilus influenza type b (3); Hepatitis B (3); Varicella; Pneumococcal; Hepatitis A (1); Influenza (2); Rotavirus (≥2). 1,2.
Combination-7 includes all the above except for flu2.
Estimates derived using general estimating equations logistic regression and robust sandwich variance estimation for clustering within child’s primary clinic. Adjusted regression included covariates for child’s insurance type and number of chronic conditions, U.S. region, and parent covariates for age on child’s second birthday, race/ethnicity, language, poverty level, insurance type, number of chronic conditions, and number of visits during the study period.
Analyses stratified by parent utilization suggest an upward trend in the association between parent and child vaccination status as number of parent visits increase, with some exceptions (Appendix Table A4). Direction, magnitude, and statistical significance were similar for estimates derived by models stratifying on number of child visits (results not shown).
4. Discussion
In this linked cohort of children and parents seen in CHCs, we found children of parents who received a flu vaccine were nearly twice as likely to be fully vaccinated by age two, but association strength differed based on parent sample. Children linked to two parents who received flu vaccinations had more than twice the odds of being fully vaccinated by age two with and two and a half times the odds of being fully vaccinated except flu vaccine compared to children with two parents who did not receive flu vaccines. Thus, the association was highest among children that linked to two parents who both received a flu vaccine compared to children who linked only to a mother or a father. This study also highlighted a bigger association in the mother only compared to the father only sample. These results suggest parental vaccine status influences their child’s vaccine status and that the relationship is more pronounced for mothers and two parents, than for fathers. These findings are not necessarily surprising since parents decide when and if they will vaccinate their children and it is likely that parents willing to receive a vaccination themselves believe in their utility, but do confirm the relationship. These findings confirm priors studies of parent reported concordance between vaccinating themselves and their children [17,20,21].
Previous suggestions to improve child vaccination rates include removing sociodemographic barriers, addressing misinformation, effective communication between clinician and patient [29], and addressing vaccine hesitancy with parents [30]. Our results suggest that another strategy to increase child vaccination rates could be increasing parent vaccination efforts. Since previous studies reflect that most adults would get a vaccine if their healthcare provider recommended it [31], making sure to recommend relevant vaccinations to parents may, in turn, increase child vaccination rates. This is particularly important in the current environment, as the COVID-19 vaccine was recently approved for children [32]. Continuing to appeal to parents on vaccine efforts may have a positive impact on uptake of COVID-19 vaccination for their children. Indeed, COVID-19 vaccine-willing parents were much more likely to have vaccinated their children, if eligible, than vaccine-hesitant parents [33,34]. In addition to the need to identify ways to ensure that children receive COVID-19 vaccines, there is urgency to increase guideline-concordant vaccination rates for children up to age two. After declining ~22% during the pandemic, vaccination rates for children under age 2 are increasing but not yet up to pre-pandemic levels [35]. Prior to the pandemic, parental vaccine hesitancy was recognized as a factor in low vaccination rates among some children [18,19], and it is possible that COVID-19 vaccine hesitancy will impact receipt of other childhood vaccinations. This potential phenomenon should be the topic of future research. In addition, we should align research of children’s vaccination status with what is happening with parent vaccination status.
Of note, our fully vaccinated (combination 10) rates were likely low because our cohort consists of patients seen in CHCs who were either uninsured or Medicaid insured, which is associated with lower vaccination rates than children with private coverage [13]. Previous data by insurance type showed rates of children fully vaccinated by age two were 57.9% for commercial health maintenance organization (HMO) insured children and 38.1% of children with Medicaid HMO insurance [8]. Previous research also showed flu vaccine for children by age two is particularly low [27]. In addition, parents report more hesitancy with flu vaccine (25.8%) than for other recommended childhood vaccines (6.1%) [36]. These findings were echoed by our study: the percentages of children who received all vaccines except flu (combination 7) were substantially higher than those with flu vaccine included. The CDC reported a combination 7 rate of 70.5% in 2019 [27], which is close to the rates in our mother only and two parent samples.
4.1. Limitations
This is a study of association among a linked cohort of children and parents both seen in the same CHC network, which may not be generalizable to all children or all settings. Linking parents and children in EHR data is imperfect and could have led to missing links. In addition, we did not include different family types, such as grandparents acting as parents. This study was limited to children and parents with an EHR as a patient, thus informed presence bias is possible. Children were considered fully vaccinated for Hib with 3 or more documented doses as our data were lacking brand names to differentiate between 3 and 4 dose Hib series. However, our method follows the Core Set of Children’s Health Care Quality Measures for Medicaid and the Children’s Health Insurance Program technical specifications for reporting immunization status, including guidelines for Hib [2]. We included a measure of childhood vaccinations recommended by the age of two, but some children may receive vaccination outside this window. That said, the important findings here are the relationship between parent and child vaccination and not necessarily the actual vaccination rates, which are low compared to national averages but similar to averages for children with Medicaid insurance. We report increasing flu vaccination rates over time; one reason for this may be due to missing data in the earlier years improved by better data capture in the later years. There are also several reasons for potential missing vaccination data at the patient-, clinic-, and state-levels. Although we were limited in our ability to account for state differences in reporting policies and/or interoperability of vaccine reporting systems between clinic and state, we utilized several methods to account for the variability of potential missing vaccination data at the patient- and clinic-levels, including covariate adjusting, stratified sensitivity analyses, and clustering of standard errors. While the stratified findings support our general conclusions, misclassification bias is still possible. Moreover, our clustering on clinics may have reduced any state-level effects since clinics are nested within states. Lastly, this study did not assess causation but rather association between parent and child vaccinations.
5. Conclusions
Children with a parent that received a flu vaccine were nearly twice as likely to be fully vaccinated by age two compared to children with a parent that did not receive a flu vaccine. The likelihood was even higher for children with two parents who both received a flu vaccine compared to no flu vaccine for either parent. These findings suggest an additional strategy to increase childhood vaccination could be to try to increase parent vaccination.
Acknowledgments
This work was conducted with the Accelerating Data Value Across a National Community Health Center Network (ADVANCE) Clinical Research Network (CRN). ADVANCE is led by OCHIN in partnership with Health Choice Network, Fenway Health, and Oregon Health & Science University. ADVANCE is funded through the Patient-Centered Outcomes Research Institute (PCORI), contract number RI-OCHIN-01-MC.
This work was supported by Agency for Healthcare Research and Quality [grant #R01HS025962]. The Agency for Healthcare Research and Quality had no role in the design or conduct of this study.
This study was approved by the Oregon Health and Science University Institutional Review Board [ID#: STUDY00019958].
Dr. Angier conceptualized and designed the study, drafted the initial manuscript, provided data interpretation, and reviewed and revised the manuscript. Dr. Kaufmann carried out the initial analyses, provided initial data interpretation, drafted initial manuscript, and reviewed and revised the manuscript. Ms. Moreno coordinated data collection and analyses and reviewed and revised the manuscript. Ms. Cahen provided data interpretation and reviewed and revised the manuscript. Dr. DeVoe provided data interpretation, clinical contextual expertise, and reviewed and revised the manuscript. Dr. Marino supervised initial analyses, provided data interpretation, and reviewed and revised the manuscript. All authors approved the final manuscript as submitted and agree to be accountable for all aspects of the work. All authors attest they meet the ICMJE criteria for authorship.
Appendix A
Table A1.
Characteristics of father-only sample, child having had at least one ambulatory visit between the ages of 12 – 24 months (2009–2018).
| Group, No. (%) | |||
|---|---|---|---|
| Parent Had >=1 Flu Vaccine During Study Period | |||
| Parent Characteristics | All | No | Yes |
| N = 2784 | N = 1853 | N = 931 | |
| Age at Child’s 2nd Birthday | median = 34, range:14–57 | median = 33, range:16–57 | median = 35, range:14–56 |
| Race and Ethnicity | |||
| Hispanic | 677 (24.3%) | 473 (25.5%) | 204 (21.9%) |
| Non-Hispanic White | 1251 (44.9%) | 902 (48.7%) | 349 (37.5%) |
| Non-Hispanic Black | 246 (8.8%) | 157 (8.5%) | 89 (9.6%) |
| Non-Hispanic Other | 417 (15.0%) | 198 (10.7%) | 219 (23.5%) |
| Unknown | 193 (6.9%) | 123 (6.6%) | 70 (7.5%) |
| English Language Preferred | 1515 (54.4%) | 1132 (61.1%) | 383 (41.1%) |
| Last Known Insurance Status | |||
| Private | 673 (24.2%) | 508 (27.4%) | 165 (17.7%) |
| Public | 1487 (53.4%) | 889 (48.0%) | 598 (64.2%) |
| Uninsured | 624 (22.4%) | 456 (24.6%) | 168 (18.0%) |
| Unresolved Chronic Conditions a | |||
| 0 | 1661 (59.7%) | 1192 (64.3%) | 469 (50.4%) |
| 1 | 522 (18.8%) | 324 (17.5%) | 198 (21.3%) |
| >1 | 601 (21.6%) | 337 (18.2%) | 264 (28.4%) |
| Visits During Study | |||
| 0 | 677 (24.3%) | 618 (33.4%) | 59 (6.3%) |
| 1 | 656 (23.6%) | 434 (23.4%) | 222 (23.8%) |
| 2–4 | 900 (32.3%) | 549 (29.6%) | 351 (37.7%) |
| 5+ | 551 (19.8%) | 252 (13.6%) | 299 (32.1%) |
| Child Characteristics | |||
| Female | 1294 (46.5%) | 854 (46.1%) | 440 (47.3%) |
| Last Known Insurance Status | |||
| Private | 506 (18.2%) | 377 (20.3%) | 129 (13.9%) |
| Public | 2063 (74.1%) | 1315 (71.0%) | 748 (80.3%) |
| Uninsured | 215 (7.7%) | 161 (8.7%) | 54 (5.8%) |
| Last Known Federal Poverty Level | |||
| <=138% | 1823 (65.5%) | 1153 (62.2%) | 670 (72.0%) |
| >138% | 427 (15.3%) | 305 (16.5%) | 122 (13.1%) |
| Not Documented | 534 (19.2%) | 395 (21.3%) | 139 (14.9%) |
| Unresolved Chronic Conditions a | |||
| 0 | 2360 (84.8%) | 1583 (85.4%) | 777 (83.5%) |
| 1+ | 424 (15.2%) | 270 (14.6%) | 154 (16.5%) |
| Visits During Study | |||
| 1 | 390 (14.0%) | 270 (14.6%) | 120 (12.9%) |
| 2–3 | 540 (19.4%) | 371 (20.0%) | 169 (18.2%) |
| 4–8 | 725 (26.0%) | 517 (27.9%) | 208 (22.3%) |
| 9+ | 1129 (40.6%) | 695 (37.5%) | 434 (46.6%) |
| Region b | |||
| Northeast | 181 (6.5%) | 102 (5.5%) | 79 (8.5%) |
| South | 19 (0.7%) | 17 (0.9%) | 2 (0.2%) |
| Midwest | 297 (10.7%) | 182 (9.8%) | 115 (12.4%) |
| West | 2287 (82.1%) | 1552 (83.8%) | 735 (78.9%) |
Flu = influenza vaccine.
The number of chronic conditions listed in the patient’s problem list that are unresolved as of study end.
States include: Northeast (MA); South (FL, GA, NC, TX); Midwest (IN, MN, OH, WI); West (AK, CA, MT, NV, OR, UT, WA).
Table A2.
Characteristics of two-parent sample, child having had at least one ambulatory visit between the ages of 12 – 24 months (2009–2018).
| Group, No. (%) | ||||
|---|---|---|---|---|
| Parents with >=1 Flu Vaccine During Study Period | ||||
| Parent Characteristics | All | None | One | Both |
| N = 1779 | N = 655 | N = 667 | N = 457 | |
| P1 Age at Child’s 2nd Birthday | median = 31, range:14–57 | median = 31, range:14–57 | median = 31, range:14–55 | median = 32, range:14–57 |
| P2 Age at Child’s 2nd Birthday | median = 31, range:13–57 | median = 31, range:15–57 | median = 31, range:13–57 | median = 32, range:15–57 |
| Same Sex Couple | 173 (9.7%) | 50 (7.6%) | 86 (12.9%) | 37 (8.1%) |
| Race and Ethnicity | ||||
| Hispanic | 657 (36.9%) | 170 (26.0%) | 335 (50.2%) | 152 (33.3%) |
| Non-Hispanic White | 520 (29.2%) | 270 (41.2%) | 136 (20.4%) | 114 (24.9%) |
| Non-Hispanic Black | 116 (6.5%) | 35 (5.3%) | 49 (7.3%) | 32 (7.0%) |
| Non-Hispanic Other | 198 (11.1%) | 40 (6.1%) | 57 (8.5%) | 101 (22.1%) |
| Different Race and Ethnicity | 278 (15.6%) | 135 (20.6%) | 89 (13.3%) | 54 (11.8%) |
| Unknown | 10 (0.6%) | 5 (0.8%) | 1 (0.1%) | 4 (0.9%) |
| English Language Preferred | 935 (52.6%) | 453 (69.2%) | 314 (47.1%) | 168 (36.8%) |
| Last Known Insurance Status | ||||
| Both Private | 144 (8.1%) | 73 (11.1%) | 41 (6.1%) | 30 (6.6%) |
| Both Public | 734 (41.3%) | 244 (37.3%) | 240 (36.0%) | 250 (54.7%) |
| One Private | 194 (10.9%) | 81 (12.4%) | 77 (11.5%) | 36 (7.9%) |
| One Public | 330 (18.5%) | 125 (19.1%) | 138 (20.7%) | 67 (14.7%) |
| Both Uninsured | 377 (21.2%) | 132 (20.2%) | 171 (25.6%) | 74 (16.2%) |
| P1 Unresolved Chronic Conditionsa | ||||
| 0 | 936 (52.6%) | 405 (61.8%) | 328 (49.2%) | 203 (44.4%) |
| 1 | 378 (21.2%) | 125 (19.1%) | 148 (22.2%) | 105 (23.0%) |
| >1 | 465 (26.1%) | 125 (19.1%) | 191 (28.6%) | 149 (32.6%) |
| P2 Unresolved Chronic Conditionsa | ||||
| 0 | 962 (54.1%) | 412 (62.9%) | 346 (51.9%) | 204 (44.6%) |
| 1 | 381 (21.4%) | 108 (16.5%) | 155 (23.2%) | 118 (25.8%) |
| >1 | 436 (24.5%) | 135 (20.6%) | 166 (24.9%) | 135 (29.5%) |
| P1 Visits During Study | ||||
| 0 | 383 (21.5%) | 189 (28.9%) | 165 (24.7%) | 29 (6.3%) |
| 1 | 231 (13.0%) | 98 (15.0%) | 84 (12.6%) | 49 (10.7%) |
| 2–4 | 487 (27.4%) | 178 (27.2%) | 176 (26.4%) | 133 (29.1%) |
| 5+ | 678 (38.1%) | 190 (29.0%) | 242 (36.3%) | 246 (53.8%) |
| P2 Visits During Study | ||||
| 0 | 374 (21.0%) | 210 (32.1%) | 143 (21.4%) | 21 (4.6%) |
| 1 | 218 (12.3%) | 95 (14.5%) | 83 (12.4%) | 40 (8.8%) |
| 2–4 | 485 (27.3%) | 176 (26.9%) | 172 (25.8%) | 137 (30.0%) |
| 5+ | 702 (39.5%) | 174 (26.6%) | 269 (40.3%) | 259 (56.7%) |
| Child Characteristics | ||||
| Female | 851 (47.8%) | 305 (46.6%) | 325 (48.7%) | 221 (48.4%) |
| Last Known Insurance Status | ||||
| Private | 158 (8.9%) | 90 (13.7%) | 38 (5.7%) | 30 (6.6%) |
| Public | 1535 (86.3%) | 524 (80.0%) | 603 (90.4%) | 408 (89.3%) |
| Uninsured | 86 (4.8%) | 41 (6.3%) | 26 (3.9%) | 19 (4.2%) |
| Last Known Federal Poverty Level | ||||
| <=138% | 1361 (76.5%) | 467 (71.3%) | 520 (78.0%) | 374 (81.8%) |
| >138% | 300 (16.9%) | 123 (18.8%) | 113 (16.9%) | 64 (14.0%) |
| Not Documented | 118 (6.6%) | 65 (9.9%) | 34 (5.1%) | 19 (4.2%) |
| Unresolved Chronic Conditions a | ||||
| 0 | 1412 (79.4%) | 554 (84.6%) | 499 (74.8%) | 359 (78.6%) |
| 1+ | 367 (20.6%) | 101 (15.4%) | 168 (25.2%) | 98 (21.4%) |
| Visits During Study | ||||
| 1 | 85 (4.8%) | 53 (8.1%) | 20 (3.0%) | 12 (2.6%) |
| 2–3 | 152 (8.5%) | 87 (13.3%) | 36 (5.4%) | 29 (6.3%) |
| 4–8 | 386 (21.7%) | 187 (28.5%) | 127 (19.0%) | 72 (15.8%) |
| 9+ | 1156 (65.0%) | 328 (50.1%) | 484 (72.6%) | 344 (75.3%) |
| Region b | ||||
| Northeast | 85 (4.8%) | 11 (1.7%) | 42 (6.3%) | 32 (7.0%) |
| South | 3 (0.2%) | 2 (0.3%) | 1 (0.1%) | 0 (0.0%) |
| Midwest | 95 (5.3%) | 16 (2.4%) | 31 (4.6%) | 48 (10.5%) |
| West | 1596 (89.7%) | 626 (95.6%) | 593 (88.9%) | 377 (82.5%) |
Flu = influenza vaccine.
The number of chronic conditions listed in the patient’s problem list that are unresolved as of study end.
States include: Northeast (MA); South (FL, GA, NC, TX); Midwest (IN, MN, OH, WI); West (AK, CA, MT, NV, OR, UT, WA).
Table A3.
Unadjusted prevalence of child and parent vaccination status by year child turned age two years stratified by parent sample.
| Group, member vaccination % | ||||||||||
|---|---|---|---|---|---|---|---|---|---|---|
| Mothers Only Group |
Fathers Only Group |
Two Parents Group |
||||||||
| Yeara | Child comb.10 | Child comb.7 |
Parent
flu |
Child comb.10 | Child comb.7 |
Parent
flu |
Child comb.10 | Child comb.7 | 1 Parent flu | 2 Parents flu |
| 2009 | 14.4 | 37.1 | 32.9 | 16.2 | 29.4 | 11.8 | 25.6 | 47.8 | 35.6 | 11.1 |
| 2010 | 17.4 | 53.7 | 33.5 | 11.3 | 41.8 | 14.9 | 25.8 | 50.0 | 38.3 | 6.3 |
| 2011 | 22.2 | 60.5 | 37.2 | 15.6 | 43.6 | 19.6 | 22.5 | 55.1 | 37.4 | 18.7 |
| 2012 | 25.4 | 59.7 | 43.2 | 15.1 | 40.2 | 21.5 | 19.0 | 57.0 | 39.2 | 13.3 |
| 2013 | 25.6 | 60.6 | 49.7 | 21.0 | 43.3 | 28.6 | 20.9 | 62.8 | 33.0 | 19.9 |
| 2014 | 26.6 | 64.1 | 52.0 | 18.9 | 47.8 | 28.5 | 19.3 | 60.2 | 39.2 | 29.2 |
| 2015 | 24.7 | 63.6 | 53.3 | 13.5 | 41.1 | 32.9 | 27.3 | 61.5 | 44.9 | 27.8 |
| 2016 | 25.9 | 65.6 | 56.1 | 20.9 | 47.1 | 34.7 | 21.6 | 54.7 | 37.9 | 31.6 |
| 2017 | 27.6 | 65.2 | 56.0 | 19.5 | 40.5 | 43.9 | 23.8 | 56.7 | 30.7 | 39.8 |
| 2018 | 28.4 | 58.6 | 58.6 | 21.3 | 39.8 | 44.9 | 28.9 | 54.9 | 39.4 | 37.0 |
Flu = influenza vaccine.
Combination 10 vaccination (number required): Diphtheria, Tetanus, acellular Pertussis (4); Polio (3); Measles, Mumps, Rubella (1); Haemophilus influenza type b (3); Hepatitis B (3); Varicella; Pneumococcal; Hepatitis A (1); Influenza (2); Rotavirus (≥2). 1,2.
Combination-7 includes all the above except for flu2.
Prevalence shown for parents is of having received a flu vaccine during the child’s first two years of life including gestation period.
Year the child turned two years old.
Table A4.
Association between parents’ flu vaccine status and child being fully vaccinated by age two, stratified by number of parent visits during the study period.
| Child Vaccination Status, Odds Ratio (95% CI) |
||
|---|---|---|
| Fully | Fully Except Influenza | |
| Parent received influenza vaccine | (Combination 10) | (Combination 7) |
| Mother only sample | ||
| Visits during study period | ||
| 0 | 1.54 (1.30, 1.84) | 1.38 (1.12, 1.69) |
| 1 | 1.94 (1.52, 2.49) | 1.59 (1.34, 1.87) |
| 2–4 | 1.95 (1.66, 2.29) | 1.49 (1.37, 1.63) |
| 5+ | 2.17 (1.87, 2.52) | 1.50 (1.38, 1.64) |
| Father only sample | ||
| Visits during study period | ||
| 0 | 1.72 (0.80, 3.71) | 1.22 (0.62, 2.43) |
| 1 | 1.71 (1.10, 2.66) | 0.99 (0.74, 1.33) |
| 2–4 | 1.47 (1.10, 1.96) | 1.19 (0.89, 1.59) |
| 5+ | 2.44 (1.39, 4.28) | 1.60 (1.09, 2.35) |
Combination 10 vaccination (number required): Diphtheria, Tetanus, acellular Pertussis (4); Polio (3); Measles, Mumps, Rubella (1); Haemophilus influenza type b (3); Hepatitis B (3); Varicella; Pneumococcal; Hepatitis A (1); Influenza (2); Rotavirus (≥2).1,2.
Combination-7 includes all the above except for influenza2.
Estimates derived using general estimating equations logistic regression and robust sandwich variance estimation for clustering within child’s primary clinic. Adjusted for child’s insurance type and number of chronic conditions, U.S. region, and parent covariates for age on child’s 2nd birthday, race/ethnicity, language, poverty level, insurance type, and number of chronic conditions, stratified by number of parent visits during the study period.
Footnotes
Declaration of Competing Interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
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