key: cord-1013735-uvz7zsni
authors: Teasdale, Chloe A.; Borrell, Luisa N.; Shen, Yanhan; Kimball, Spencer; Zimba, Rebecca; Kulkarni, Sarah; Rane, Madhura; Rinke, Michael L.; Fleary, Sasha A.; Nash, Denis
title: Missed routine pediatric care and vaccinations in US children during the first year of the COVID-19 pandemic
date: 2022-03-19
journal: Prev Med
DOI: 10.1016/j.ypmed.2022.107025
sha: acddb223230f97591ff494b5cc32d69d8876a177
doc_id: 1013735
cord_uid: uvz7zsni

The COVID-19 pandemic has decreased uptake of pediatric preventive care, including immunizations. We estimate the prevalence of missed pediatric routine medical visits and vaccinations over the first year of the COVID-19 pandemic. We conducted a cross-sectional online survey of 2074 US parents of children ≤12 years in March 2021 to measure the proportion of children who missed pediatric care and vaccinations over the first 12 months of the COVID-19 pandemic. Poisson regression models were fitted to estimate adjusted prevalence ratios (aPR). All analyses were weighted to represent the target population. Overall, 41.3% (95%CI 38.3–43.8) of parents reported their youngest child missed a routine medical visit due to the COVID-19 pandemic. Missed care was more common among children >2 years compared to <2 years (aPR 1.82; 95%CI 1.47–2.26) and Hispanics compared to non-Hispanic Whites (aPR 1.31; 95%CI 1.14–1.51). A third of parents (33.1%; 95%CI 30.7–35.5) reported their child had missed a vaccination. Pediatric influenza vaccination decreased in the 2020–21 flu season compared to 2019–20 (51.3% vs. 62.2%; p < 0.0001). A high proportion of US children ≤12 years missed routine pediatric care during the COVID-19 pandemic. Catch-up efforts are needed to ensure continuity of preventive care for all children.

The SARS-CoV-2 (COVID- 19) pandemic has significantly disrupted the lives of adults and children in the United States (US). In March 2020, the US Centers for Disease Control and Prevention (CDC) called for social distancing and, during the first months of the pandemic, some states enacted stay at home orders. 1 Early in the pandemic, the CDC also recommended medical providers delay non-emergency and elective care to preserve the capacity of the healthcare system and to minimize transmission risk. 2 These policies, as well as personal concerns about exposure, may have resulted in lower uptake of routine pediatric medical care which could have significant long-term impact on the health of children, their families and communities.

Several studies have shown declines in vaccination uptake among children during the COVID-19 pandemic. In May 2020, the CDC reported a drop in orders from the Vaccines for Children Program (VFC) 3 which provides free immunizations to half of US children, 4 and data from immunization registries confirmed decreased vaccination uptake early in the COVID-19 pandemic. [5] [6] [7] In New York City, vaccinations for children <24 months returned to pre-COVID levels by June 2020, however uptake remained 35% lower among older children. 6 In Ohio, a decline in care visits attended by infants and young children during the first six months of the COVID-19 pandemic led to lower measles-mumps-rubella (MMR) vaccination rates. 8 There is less information about the extent of missed routine pediatric care however an analysis by the Commonwealth Fund of data from 50,000 health care providers across the US found that in March 2020, pediatric outpatient care visits declined by 70% for children <18 years and that pediatric visits remained below pre-pandemic levels by October 2020. 9 In addition, from March to May of 2020, half a million fewer US children received blood lead level screening, 10,000 of whom may have had elevated levels requiring interventions. 10 As well as highlighting J o u r n a l P r e -p r o o f Journal Pre-proof concerning gaps in vaccination coverage, these data are suggestive of significant and potentially harmful disruptions to routine pediatric preventive care as a result of the COVID-19 pandemic.

Evidence in adults suggests that missed care during the COVID-19 pandemic may have contributed to increased mortality from causes other than SARS-CoV-2. 11, 12 While the consequences of missed care for children may be less severe, they remain significant. The American Academy of Pediatrics (AAP) guidelines call for monthly visits for infants up to six months and annual wellness visits for children >2 years. 13 CDC's pediatric immunization schedule includes 15 vaccinations (plus boosters) and immunization for seasonal influenza. 14 Avoidance of pediatric care could lead to missed diagnoses of developmental delays, emotional problems, physical disabilities and other conditions identified through routine screening. Missed vaccinations could have serious consequences for the health of children and communities and contribute to outbreaks of vaccine-preventable illnesses. [15] [16] [17] There are few data on the prevalence of missed care visits among US children and little information about which children are at highest risk. In order to quantify the prevalence of missed routine pediatric preventive care as a result of the COVID-19 pandemic, including receipt of vaccinations, and to identify the characteristics of children at risk for missed care, we conducted an online survey of US parents of children <12 years.

The cross-sectional survey of parents and caregivers ('parents') of children <12 years from across the US was conducted from March 9 through April 2, 2021. Participants were English and Spanish speaking adults >18 years who identified as a primary caregiver of a child <12 years J o u r n a l P r e -p r o o f Journal Pre-proof who had taken the child to a medical visit in the past two years. The sample was recruited via Qualtrics, an online survey administration service maintaining a database of millions of US participants across multiple non-probability survey panels identified through social media platforms and parent networks (ie, business-to-business partners used by Qualtrics). 18 We followed guidelines from the American Association for Public Opinion Research (AAPOR) 19 and Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) for crosssectional studies. 20 The survey instrument was developed for this study with questions modeled on the 2020 National Survey of Children's Health. 21 The study was approved by the City University of New York (CUNY) Graduate School of Public Health institutional review board.

Proportionate sampling based on sex, race, ethnicity, education and US region was utilized to weight the sample to the target population of US parents of children <12 years according to 2019 US Census data. 22 The target sample size was 2,000 to obtain precise estimates for race/ethnicity groups; the final sample included 2,074 participants. Respondents were recruited online through social media platforms and partner networks using standard procedures 18 ; individuals opting in were linked to the anonymous online survey. After completing screening questions, eligible participants provided medical care and vaccination information about the youngest child in the household (in order to achieve an adequate sample of younger children), as well as sociodemographic questions about the parent and household. (eAppendix) All data were de-identified.

In accordance with the AAPOR guidelines for reporting opt-in non-probability panel data, participation rates cannot be estimated as the sampling frame is unknown. 19

The primary outcomes were prevalence of missed routine care visits and missed routine vaccinations (not including influenza) in children since the start of the COVID-19 pandemic as J o u r n a l P r e -p r o o f Journal Pre-proof reported by parents. The survey asked, "Have you avoided scheduling or cancelled a scheduled routine well visit (check-up) for the child because of the COVID-19 epidemic?" and "Has your child's pediatrician or medical care provider contacted you to tell you or are you aware that your child is due for a vaccine, missed a vaccination or needs to catch up on vaccines? This does not include flu vaccine". The wording of this question differed from missed visits as most parents may be unaware of when their child is due for a vaccination until it has been missed and they are notified by a care provider. Response options for both questions were yes, no, don't know and

prefer not to answer. (eAppendix) Secondary outcomes included whether the child attended a medical visit following missed care (i.e. make-up visit) and whether the parent planned to take the child to get a missed vaccination.

Parents reporting missed visits and vaccinations were asked to select the primary reason for missed care from a list of options. Secondary outcomes also included where the child had attended medical care since the start of the COVID-19 pandemic (with multiple response options) and whether the child had received influenza vaccinations in the 2019-20 and 2020-21 flu seasons (measured as an additional indicator of missed care).

Parents reported demographic information for the child and themselves, including age and race/ethnicity, as well as information about whether the child had health insurance covering some or all doctor visit costs, and whether the child was attending in-person school or daycare >1 day per week. Race and ethnicity were asked as separate questions. We report outcomes for the largest race/ethnicity groups and include a 'non-Hispanic other' category which includes anyone not identified as Hispanic, Latino/a or Spanish origin, and reporting race as American Indian, Alaska Native, Pacific Islander or 'other'. Child's age was calculated based on reported month and year of birth (using the first of the month for all birthdates) and age groups were J o u r n a l P r e -p r o o f based on the CDC's immunization schedule which includes more vaccinations for children <6 years compared to those >7 years 14 (we further divided the younger group to examine children <2 years). Information on the household included the number of children 0-12 years of age, household income and region of the US (based on reported zip code).

Descriptive statistics on the sample population are presented as raw frequencies and weighted percentages. Prevalence estimates for study outcomes are shown as proportions with 95% confidence intervals (CI) and were examined overall, and by the child's race/ethnicity (non-Hispanic (NH) Black, Asian, NH White, Hispanic and NH Other) and age group (<2 years, 2-6 years and 7-12 years). Rao-Scott adjusted Pearson chi-square tests were used to compare prevalence of outcomes across race/ethnicity and age groups.

Poisson regression models with robust standard errors were fitted to estimate adjusted prevalence ratios for each outcome and included demographic characteristics of the child, parent and household (parent race was excluded from adjusted models due to collinearity with child's race).

Parents reporting "don't know" or "prefer not to answer" for missed care (N=43) or missed vaccinations (N=95) were excluded from regression models. To examine potential bias from these exclusions, we ran models including parents reporting "don't know" or "prefer not to answer" with the "yes" and "no" groups for each outcome (estimates did not change). All levels of demographic characteristics in the models were included but some were not reported due to small sample size, and thus, unreliable estimates. Analyses were conducted in SAS 9.4 (SAS Institute Inc., Cary, NC, USA). In adjusted models, compared to children <2 years, those 2-6 years (aPR 1.82; 95%CI 1.47-2.26) and 7-12 years (aPR 1.86; 95%CI 1.48-2.33) were more likely to have a missed visit due to the COVID-19 pandemic (Table 3) . Hispanic children were also more likely to have missed visits compared to NH White children (aPR 1.31; 95%CI 1.14-1.51). Parents with three or more children were more likely to report missed visits compared to those with one child (aPR 1.24; 95%CI 1.03-1.49) while parents with income $25,000-$49,000 were less likely to report missed care compared to those with income >$100,000 (aPR 0.76; 95%CI 0.63-0.91) ( Table 3 ). In separate adjusted models, female parents were less likely to report missed vaccinations for children compared to male parents (aPR 0.72; 95%CI 0.62-0.84), while parents in the Western J o u r n a l P r e -p r o o f region of the US were more likely to report missed vaccinations compared to other regions (aPR 1.47; 95%CI 1.21-1.78) ( Table 3) .

Most parents (71.2%; 95%CI 68.9-73.6) reported their child had attended an in-person medical care visit since the start of the COVID-19 pandemic, 29.8% (95%CI 27.6-32.1) reported a telemedicine visit, and 10.0% (95%CI 8.4-11.6) reported their child had received no medical care (Figure 1 ). Attendance at in-person care visits was more common among children <2 years (83.3%; 95%CI 77.9-88.8) compared to 7-12-year-old children (63.3%; 95%CI 59.6-67.0) (p<0.001) while older children (7- p=0.03).

The COVID-19 pandemic has disrupted routine pediatric medical care, including vaccinations.

In our survey of US parents conducted in March 2021, more than 40% reported that their youngest child had missed a routine medical care visit as a result of the COVID-19 pandemic but most children (79%) subsequently attended catch-up care. A third (33.1%) of US parents also reported that their child had missed a required vaccination and only 65% said they planned to take the child to receive the needed vaccine. Our findings on missed care and vaccination during the COVID-19 pandemic are consistent with the few studies to date assessing its impact on uptake of routine pediatric preventive care. 8, 9 Most existing reports have focused on vaccination uptake and showed steep declines in the early months of the pandemic with indications of catch-J o u r n a l P r e -p r o o f up, primarily in younger children, by mid-2020. [5] [6] [7] [8] 23 Our study measured any event of missed care or vaccination since the start of the pandemic, thus we cannot comment on changes in rates of missed care over the course of the pandemic. However, our finding that most children who missed a visit subsequently attended care is suggestive of the same dynamic.

While many parents reported catch-up after missed care, almost a quarter said their child had not received care following a missed visit, and this was more likely among children older than 2 years and in Hispanic children. Pediatric preventive care or "well visits", particularly for infants and young children, are important not only for assessing physical health and providing vaccinations 8 , but also for conducting screening to mark developmental milestones and identify emotional and social issues. 13 While our data are reassuring in suggesting that most infants and younger children received recommended care, older children appear at higher risk for missed care. Studies conducted prior to the pandemic have also shown that older children and Hispanic children are less likely to attend recommended annual wellness visits. 24, 25 Our findings may be an indication that the COVID-19 pandemic has exacerbated these trends which is concerning and should be examined further.

We also found high prevalence of missed vaccination which may be an underestimate given that not all parents may have been notified about a child's missed vaccination. High levels of vaccination are needed to prevent outbreaks of diseases including measles and pertussis. Our data, along with reports from vaccine registries showing decreased vaccination uptake and coverage 5-7 are very concerning, particularly as the US returns to pre-pandemic activities, including in-person education for most US children in the fall of 2021. The easing of social distancing could fuel outbreaks of vaccine-preventable illnesses among unvaccinated children. 15, 26, 27 In addition, while influenza activity (diagnoses, hospitalization and deaths) was J o u r n a l P r e -p r o o f significantly lower in 2020-21 compared to previous years, likely due to COVID-19 mitigation efforts, 28 the drop in flu vaccinations we observed among children is troubling. Our data are consistent with a CDC report showing influenza vaccine doses administered to children 6-23 months were 13.9% lower and to 2-4 year olds were 11.9% lower from September through December 2020 compared to the same months in 2018 and 2019. 29 Prior to the COVID-19

pandemic, influenza vaccination rates in US children had stalled 30, 31 and the pandemic may have eroded the progress made over the past decades. We also found that among parents who said their child had missed a vaccine but did not plan to take the child to get it, almost 20% said it was because they did want the child to get the vaccine. These findings are not a direct measure of vaccine hesitancy and we do not have data on vaccine hesitancy prior to the COVID-19 pandemic, however it is important to note that a small number of studies have documented increases in parental vaccine hesitancy during the COVID-19 pandemic which is very concerning. 32 pandemic and we cannot comment on trends over time. Our survey focused on children 12 years of age and younger in an effort to sample younger children, and thus, we do not have data on adolescents. The survey data were self-reported by parents and caregivers and is therefore subject to recall, response and social desirability biases. In addition, while our survey was weighted to reflect the US population of parents based on 2019 census estimates, it was conducted online through opt-in panels which excludes parents without internet access.

However, data from the National Center for Education Statistics show that in 2019, 95% of US children and adolescents <18 years had home internet access. 34 Finally, our information on missed vaccinations is limited as parents and caregivers may not be aware of when children are due for vaccines and pediatric practices may not have contacted parents to alert them to missed vaccinations. We did not verify reports with medical records, however previous validation of self-reported influenza vaccination with medical records has shown high agreement. 35

Our study contributes to a greater understanding of how the COVID-19 pandemic has affected J o u r n a l P r e -p r o o f 

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a Survey weights applied to sample to represent US population of parents by race, ethnicity, sex, education and region

Pearson Chi-squared tests to compare expected to observed frequencies among groups by characteristic for parent's willingness to vaccinate their youngest child (i.e. whether willing to vaccinate youngest child differed by sex of the child

c Categories are not presented in the table as they yielded unreliable standard error estimates

Acknowledgments: This study was funded by the CUNY Institute for Implementation Science in

☒ 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.☐The authors declare the following financial interests/personal relationships which may be considered as potential competing interests:J o u r n a l P r e -p r o o f