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The American Academy of Pediatrics and the Advisory Committee on Immunization Practices of the Centers for Disease Control and Prevention recommend routine human papillomavirus (HPV) vaccination for all children starting at 9 years of age. For healthy children initiating HPV vaccination before their 15th birthday, the recommended schedule is 2 doses, with the second dose administered 6–12 months after the first dose.1 Vaccination past the age of 15 years requires a 3-dose series.2,3
HPV vaccination rates were nationally low before the novel coronavirus 2019 (COVID-19) pandemic, owing to both provider and parental barriers.4 Parental barriers include a low perceived risk of HPV infection, potential adverse effects of the vaccine, and concerns that the vaccine will encourage younger children to engage in sexual activity.5 Studies have demonstrated deficiencies in the strength and quality of clinician recommendations, physician knowledge of the vaccine, and provider comfort levels with discussing sexuality.5 Misinformation from the Internet and the failure of clinicians to routinely recommend the vaccine have also contributed to low vaccine acceptance.5,6
During the COVID-19 pandemic, routine childhood vaccines were delayed or completely deferred due to many factors, including shifts in healthcare resources, quarantining and transportation challenges.7 In addition, there was an eruption of “vaccine phobia,” or fear and distrust in the efficacy of vaccination. These fears were likely rooted in the uncertainty associated with the novel strain of coronavirus, alongside economic anxiety.8 The pandemic further exacerbated barriers to vaccination that will likely persist beyond the COVID-19 outbreak. This study specifically examines the impact of COVID-19 on HPV vaccination rates in the United States.
MATERIALS AND METHODSThe New York University (NYU) Langone Institutional Review Board approved this study. A retrospective chart review was performed comparing HPV vaccination rates from March 1, 2018 to February 28, 2020 (defined as the “prepandemic” period) to HPV vaccination rates from March 1, 2020 to February 28, 2022 (“pandemic” period). COVID-19 lockdown in New York State began in March 2020, when New York saw its first rise in COVID-19 cases.9
All children 9–14 years of age with a visit of any type (sick and well) to an NYU-affiliated facility during these time periods were included in this study. The total number of visits decreased uniformly during the study period. Subjects were identified using an Epic Clarity Report (Version IU4: Epic, Inc., Verona, WI). Each subject was counted once. Subjects who spanned the 2 defined time periods (receiving the first dose of the HPV vaccine “prepandemic” and the second dose of the HPV vaccine during the “pandemic”) were excluded.
The primary outcome was the percentage of children achieving full HPV vaccination by their 15th birthday during the defined time periods. The percentage of children receiving at least 1 dose of HPV vaccine was also examined; the denominator was defined as all children 9–14 years of age to an NYU-affiliated facility during the above time periods, and the numerator was defined as the subset of this population receiving 1 or 2 doses of HPV vaccine. We aimed to further subcategorize HPV vaccination rates by age. Each subject was only included once, in one age group, defined by their most recent appointment during their specified “prepandemic” or “pandemic” grouping.
We aimed to identify a correlation between peaks in COVID-19 positivity and decreased HPV vaccination rates. The number of new positive COVID-19 cases was obtained through data from the New York State Department of Health for counties served by our hospital system, including Nassau County, Long Island, and New York City.
The rate of HPV vaccination was compared overall and separately by time period using the χ2 test. A result was considered statistically significant at the P < 0.05 level of significance. All analyses were performed using SAS version 9.4.10
RESULTSAs seen in Figure 1, a total of 41,812 patients were identified, 24,486 (56.3%) of whom did not receive any dose of the HPV vaccine over the time periods covered in this study.
FIGURE 1.: Flow chart describing the selection process of eligible study patients.
In comparing prepandemic to pandemic HPV vaccination rates, a significant difference was identified. A total of 49.3% (n = 10,344) patients received at least 1 dose of the vaccine prepandemic, compared with 33.5% (n = 6,982) during the pandemic, P < 0.0001. (Table 1) As the total number of patients receiving 2 doses of vaccine was a subset of those receiving 1 dose, it was determined that 15.7% (n = 3,313) patients received only 1 dose of vaccine prepandemic, and 14.5% (n = 3,017) patients received 1 dose of vaccine during the pandemic (no significant difference).
TABLE 1. - Breakdown of Subjects by Age Receiving Any Dose of HPV Vaccine Pre-pandemic and During the Pandemic Prepandemic (n = 20,996) Age n (total) No HPV vaccine 1st dose HPV vaccine % 1st dose HPV vaccine Full HPV vaccination (2 doses) % 2 doses HPV vaccine P value* 9 3223 2767 456 14.2 86 2.7 10 3460 2661 799 23.1 324 9.4 11 3641 1970 1671 45.9 831 22.8 12 3488 1343 2145 61.5 1417 40.6 13 3447 1060 2387 69.3 1935 56.1 14 3737 851 2886 77.2 2438 65.2 Total 20,996 10,652 10,344 7031 <0.0001 Pandemic*P value obtained using a χ2 test.
HPV indicates human papillomavirus.
A significant decrease in the number and percentage of patients receiving the full HPV series (2 doses) was observed during the pandemic: 33.5% (n = 7,031) of patients received 2 doses of HPV vaccine prepandemic, compared with 19.0% (n = 3,965) during the pandemic, P < 0.0001. Prepandemic, 65.2% (n = 2438) of 14-year-olds achieved full vaccination compared with only 16.6% (n = 609) during the pandemic (Table 1).
A positive correlation was appreciated between age and the number of patients fully vaccinated for HPV prepandemic. During the pandemic, the peak age group(s) representing fully vaccinated patients were 11- and 12-year-olds. Prepandemic, 14-year-olds, followed by 12- and 13-year-olds, represented the highest populations of fully vaccinated children (Table 1). Each subject was only included once, in one age group, defined by their most recent visit during their specified period, “prepandemic” or “pandemic.”
Figure 2 illustrates the inverse relationship between COVID-19 cases and doses of HPV vaccine administered. As the 2 variables are on different scales (number of COVID-19 cases in the hundred thousands vs. number of HPV vaccines in the hundreds), the left axis corresponds to COVID-19 and the right axis to HPV. With each spike of COVID-19 positivity, rates of HPV vaccination declined in parallel.
FIGURE 2.: Relationship between rates of HPV vaccination and number of new COVID-19 positive tests in NYC and Nassau County, NY.9 HPV indicates human papillomavirus.DISCUSSION
Before the pandemic, rates of HPV vaccination nationwide were lower than for other adolescent vaccinations.1 In 2019, among adolescents 13–17 years old in the United States, approximately 90% had at least 1 dose of the Tdap vaccine (after age 10), 89% had at least 1 dose of the meningococcal vaccine and 72% had at least 1 dose of the HPV vaccine.11 Whereas all public school districts in the United States mandate the Tdap vaccine, and many states mandate at least 1 dose of the meningococcal ACWY vaccine (covering serotypes A, C, W, and Y), the HPV vaccine is required for matriculation only in a few areas, including Rhode Island, Hawaii, Virginia, Washington, DC, and Puerto Rico.12 Lower HPV vaccination rates may also be, in part, due to a lack of uniform clinical communication from providers, changing vaccination policies, and time constraints.5
In other parts of the world, the COVID-19 pandemic did not have a substantial impact on HPV vaccination rates.13 National vaccination reports in Israel show that vaccination rates did not fall during the pandemic, likely due to factors such as government campaigns and public acceptance of the COVID-19 vaccine. Australia had no significant drop in HPV vaccination rates in 2020.13 In England, there was a drop from 88% to 59% of school-age children vaccinated; however, an Immunization Task and Finish Group was quickly put in place to implement a rise in vaccine rates to 82% in 2021.13
HPV vaccination rates further decreased during the COVID-19 pandemic, alongside other routine adolescent vaccinations.14 A significant decrease in both initiation and completion of HPV vaccination was observed during the pandemic in our study. Many factors, including quarantining and isolation, staffing shortages, shifting resources, switches to telemedicine, and transportation disruptions, played a role in this decline.15 This decline is not without potential consequence: a simulation model-based analysis predicted that an additional 2,882–6,487 cases of cervical cancer would occur over the next century because of missed HPV vaccinations during the COVID-19 pandemic.16 On the other hand, the COVID-19 pandemic had a significant impact on the sexual activity of adolescents, including a decrease in reported sexual activity.17
We observed a shift in the age groups with higher rates of full vaccination during the pandemic period. Prepandemic, the 12-, 13-, and 14-year-old age groups had the highest completed vaccination rates, while during the pandemic, 11- and 12-year-olds were more likely to be fully vaccinated. This discrepancy may, in part, be due to a lack of vaccine requirements at 9-, 10-, 13-, and 14-year well-checks (eg, the Tdap and meningococcal vaccines are given at the 11-year well-check, with a consideration for catch-up at age 12 years), and as such, well-child visits may have been skipped.
The major limitation of our study was the inability to quantify, by age, how many children received only 1 dose of vaccine. Only their most recent visit was counted, and patients were unable to be linked. Thus, it was unclear, for example, at what age a patient who received their first HPV vaccine returned for their second (as only their final visit was accounted for). As the total number of patients receiving 2 doses of vaccine was a subset of those receiving 1 dose, we could only report on the total number of patients receiving 1 dose of vaccine during each time period. Additionally, adolescents most commonly receive this vaccine from their pediatricians during annual well-child visits, which were limited due to quarantine and hesitancy to attend these appointments. Our analysis is limited by a lack of data on school closures, as these were variable throughout the state. There was also a shift during the pandemic period toward sick visits, during which routine vaccinations would not typically be given. The number of annual well-child visits was greater during the prepandemic period, which may contribute to higher vaccination rates. Other limitations of our study included the exclusion of patients receiving 1 vaccine prepandemic and 1 vaccine during the pandemic. Our search only included pediatric ambulatory practices and may have missed patients seen at family practice locations. Additionally, immunocompromised patients were not excluded, who may have required 3 doses of HPV vaccine regardless of age. Comparing the demographics of patients declining vs. receiving HPV vaccination, including race and ethnicity, might be useful in future studies.
Worldwide, the resurgence of other vaccine-preventable illnesses, such as polio and cholera, emphasizes the necessity of ongoing vaccination programs. Routine vaccinations are recommended despite lockdowns and the changing priorities of parents.18 Because many scheduled vaccinations have already been delayed, it is essential that “catch-up activities” are utilized.19 We recommend that a “catch-up” study following this study by 1–2 years would be beneficial to evaluate the efficacy of “catch-up activities.” Because other pandemics may arise in the future, it is essential to implement evidence-based interventions that can persist during these emergencies through changes to health systems.
Potential gaps in vaccination offer opportunities for provider education. Activities such as role-play to encourage providers to make strong clinical recommendations, citing the Centers for Disease Control and Prevention and the American Academy of Pediatrics, and emphasizing the various diseases and cancers caused by HPV could improve communication regarding the vaccine.20 At the Children’s Health Medical Group in Dallas, Texas, there was an increase in HPV vaccination rates despite an almost 20% decrease in visits for patients 9–22 years old. This may be due to consistent provider recommendations for the vaccine.21 Further studies will report on the implementation of HPV education and any resulting improvement in vaccination rates. In addition, school-based vaccine programs have been implemented in places such as the United Kingdom, Canada, Australia, and some parts of the United States.22 These programs help to significantly increase vaccination rates. During pandemics, drive-through vaccine clinics can be utilized to increase vaccination rates while minimizing exposure to others.
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