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Uptake of infant and preschool immunisations in Scotland and England during the COVID-19 pandemic: An observational study of routinely collected data

• Rachel Mulholland,
• Yuma Sangpang Rai,
• Utkarsh Agrawal,
• Helen Bedford,
• J. Claire Cameron,
• Cheryl Gibbons,
• Partho Roy,
• Aziz Sheikh,
• Ting Shi,
• Colin R. Simpson,
• Judith Tait,
• Elise Tessier,
• Steve Turner,
• Jaime Villacampa Ortega,
• Joanne White,
•  [ ... ],
• Rachael Woods
• [ view all ]
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Uptake of infant and preschool immunisations in Scotland and England during the COVID-19 pandemic: An observational study of routinely collected data

• Fiona McQuaid,
• Rachel Mulholland,
• Yuma Sangpang Rai,
• Utkarsh Agrawal,
• Helen Bedford,
• J. Claire Cameron,
• Cheryl Gibbons,
• Partho Roy,
• Aziz Sheikh,
• Ting Shi

ten

• Published: February 22, 2022
• https://doi.org/ten.1371/journal.pmed.1003916

Figures

Abstract

Background

In 2020, the SARS-CoV-2 (COVID-19) pandemic and lockdown control measures threatened to disrupt routine childhood immunisation programmes with early reports suggesting uptake would autumn. In response, public health bodies in Scotland and England collected national data for childhood immunisations on a weekly or monthly basis to let for rapid analysis of trends. The aim of this study was to use these data to appraise the impact of different phases of the pandemic on infant and preschool immunisation uptake rates.

Methods and findings

We conducted an observational report using routinely nerveless data for the year prior to the pandemic (2019) and immediately before (22 January to March 2020), during (23 March to 26 July), and subsequently (27 July to iv Oct) the first UK "lockdown". Information were obtained for Scotland from the Public Wellness Scotland "COVID19 wider impacts on the wellness care arrangement" dashboard and for England from ImmForm.

Five vaccinations delivered at unlike ages were evaluated; 3 doses of "vi-in-1" diphtheria, tetanus, pertussis, polio, Haemophilus influenzae blazon b, and hepatitis B vaccine (DTaP/IPV/Hib/HepB) and 2 doses of measles, mumps, and rubella (MMR) vaccine. This represented 439,754 invitations to be vaccinated in Scotland and 4.1 million for England. Uptake during the 2020 periods was compared to the previous year (2019) using binary logistic regression analysis. For Scotland, uptake within 4 weeks of a kid becoming eligible past historic period was analysed along with geographical region and indices of deprivation. For Scotland and England, we assessed whether immunisations were upwards-to-appointment at approximately six months (all doses 6-in-1) and 16 to 18 months (outset MMR) of age.

Nosotros found that uptake inside iv weeks of eligibility in Scotland for all the 5 vaccines was college during lockdown than in 2019. Differences ranged from 1.3% for first dose half-dozen-in-1 vaccine (95.3 versus 94%, odds ratio [OR] compared to 2019 1.28, 95% confidence intervals [CIs] 1.18 to one.39) to 14.three% for second MMR dose (66.1 versus 51.8%, OR compared to 2019 one.8, 95% CI ane.74 to 1.87). Significant increases in uptake were seen across all deprivation levels.

In England, fewer children due to receive their immunisations during the lockdown catamenia were up to date at half dozen months (vi-in-one) or 18 months (first dose MMR). The autumn in percentage uptake ranged from 0.five% for first 6-in-1 (95.viii versus 96.three%, OR compared to 2019 0.89, 95% CI 0.86– to 0.91) to ii.1% for tertiary 6-in-1 (86.6 versus 88.7%, OR compared to 2019 0.82, 95% CI 0.81 to 0.83).

The use of routinely collected data used in this report was a limiting factor as detailed data on potential misreckoning factors were non available and we were unable to eliminate the possibility of seasonal trends in immunisation uptake.

Conclusions

In this study, nosotros observed that the national lockdown in Scotland was associated with an increase in timely childhood immunisation uptake; however, in England, uptake vicious slightly. Reasons for the improved uptake in Scotland may include agile measures taken to promote immunisation at local and national levels during this flow and should be explored further. Promoting immunisation uptake and addressing potential vaccine hesitancy is particularly important given the ongoing pandemic and COVID-xix vaccination campaigns.

Author summary

Why was this study washed?

• Early reports from multiple countries suggested that the SARS-CoV-2 (COVID-19) pandemic and associated control measures such every bit "lockdowns" could be detrimental to routine childhood immunisation uptake.
• A fall in the number of children receiving their routine immunisations could leave the population vulnerable to multiple infectious diseases such as measles.
• Nonetheless, these reports generally just assessed the immediate effect inside a few weeks of national lockdowns, and the longer-term impact of COVID-xix control measures on routine babyhood immunisation uptake requires further evaluation.
• It is important to understand how the pandemic affected the uptake of routine babyhood immunisations in order to discover what factors influence immunisation uptake and assist plan for the futurity.

What did the researchers exercise and find?

• Information on childhood immunisation uptake is routinely collected in Scotland and England. Because of concerns about the event of the pandemic on immunisation uptake, this information was nerveless in more detail and we used this to examine what happened over the lockdown period.
• To run across if there was whatsoever change in immunisation uptake, nosotros compared the data from immediately before, during, and later on the 2020 lockdown in the United Kingdom to information from the previous year (2019).
• We found that immunisation uptake in Scotland rose significantly across lockdown, with over 7,000 more children receiving their immunisations on fourth dimension compared to the previous year. In England, there was a slight fall in uptake.

What exercise these findings hateful?

• These findings suggest that, despite early concerns, infant and preschool immunisation uptake increased in Scotland over the lockdown period.
• Nosotros do not nonetheless have enough information to determine the reasons backside this positive alter in Scotland or why uptake fell in England.
• The next step is to assess what factors may accept led to this credible increase in uptake, which could meliorate uptake of baby and preschool immunisations across the pandemic.
• Due to the type of information used, nosotros were unable to fully explore the possibility of immunisation uptake varying by the fourth dimension of twelvemonth, and some potentially of import details, such as ethnicity, were non available.

Citation: McQuaid F, Mulholland R, Sangpang Rai Y, Agrawal U, Bedford H, Cameron JC, et al. (2022) Uptake of baby and preschool immunisations in Scotland and England during the COVID-xix pandemic: An observational study of routinely collected data. PLoS Med 19(ii): e1003916. https://doi.org/x.1371/journal.pmed.1003916

Academic Editor: Lars Åke Persson, London School of Hygiene and Tropical Medicine, UNITED KINGDOM

Received: July xx, 2021; Accepted: Jan 17, 2022; Published: Feb 22, 2022

Copyright: © 2022 McQuaid et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted apply, distribution, and reproduction in any medium, provided the original writer and source are credited.

Data Availability: All relevant data are within the manuscript and its Supporting Information files and further Scottish information can be accessed via the Public health Scotland wider impacts dashboard https://scotland.shinyapps.io/phs-covid-wider-impact/. The English data used is included in the supplementary data. Whatever further queries regarding the data on ImmForm should be directed to EarlyChildhoodBaseline@phe.gov.uk. All code used in the analyses is publicly available via the EAVE II GitHub folio (https://github.com/EAVE-II).

Funding: This analysis was part of the EAVE Two project. EAVE II is funded past the Medical Research Council (MC_PC_19075), https://mrc.ukri.org/, with the support of BREATHE: the Health Data Research Hub for Respiratory Health (MC_PC_19004), https://www.hdruk.air conditioning.uk/helping-with-wellness-data/wellness-data-research-hubs/exhale, which is funded through the U.k. Enquiry and Innovation Industrial Strategy Claiming Fund and delivered through Health Information Research Great britain. The funders had no part in study design, data drove and analysis, decision to publish, or grooming of the manuscript.

Competing interests: I accept read the journal's policy and the authors of this manuscript have the following competing interests: Every bit is a member of the Scottish Regime Principal Medical Officer's COVID-19 Informational Group. As is a member of the Editorial Board of PLOS Medicine. HB is a member of the Prissy committee developing guidance on increasing vaccine uptake. CRS declares funding from the Medical Enquiry Quango, the National Institute for Health Research, Principal Scientist Office, and New Zealand Ministry building for Business, Innovation and Employment and Wellness Research Council during the conduct of this report. All other authors declare no competing interests.

Abbreviations: CI, confidence interval; COVID-19, Coronavirus Disease 2019; DTaP/IPV/Hib/HepB, diphtheria, tetanus, pertussis, polio, Haemophilus influenzae type b, and hepatitis B; HSCP, Wellness and Social Care Partnership; MMR, measles, mumps, and rubella; OR, odds ratio; SARS-CoV-ii, Severe Acute Respiratory Syndrome Coronavirus ii; SIMD, Scottish Alphabetize of Multiple Deprivation; WHO, World Health Organization

Introduction

The SARS-CoV-2 (COVID-19) pandemic and associated control measures such every bit national "lockdowns", involving varying restrictions on leaving the habitation, work, and socialising, accept had a profound bear on on daily life and the delivery of healthcare worldwide. In the Uk, a national lockdown was appear on 23 March 2020, with instructions that people should only leave their home for a express number of "essential" reasons [1]. This was accompanied by the reconfiguration of acute healthcare services to support the anticipated influx of COVID-19 patients, cancellation of most elective activeness, and pausing of screening programmes [2]. During lockdown, at that place was evidence of a change in healthcare-seeking behaviour—for example, in Scotland, the uptake of both emergency and constituent hospital-based care dropped essentially over the lockdown menstruum [3]. However, within kid wellness, key routine services including childhood immunisations continued through the UK [4].

It has become increasingly credible that younger children are at low risk of astringent disease due to Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2) [5] and may be less susceptible to infection with the virus [vi]. Yet the wider impact of the pandemic on children in terms of education, mental and physical health, and safeguarding is not withal fully understood and is likely to be profound [7,8]. One particular expanse of business organization early in the lockdown period was the potential effect on the uptake of routine childhood immunisations [ix]. Maintaining high population vaccine coverage is vital for both straight and indirect (via herd immunity) protection against non-COVID-19 infectious diseases.

In July 2020, the Globe Health Organization (WHO) warned of a potential reject in routine immunisation rates associated with the COVID-19 pandemic, citing a poll from May 2020 in which respondents from 82 countries suggested disruption to immunisation programmes was widespread [10]. Initial reports from England [xi], Pakistan [12], Due south Africa [13], Singapore [xiv], and the U.s.a. [15] were apropos, suggesting a fall in children receiving their scheduled vaccinations in the very early weeks of national lockdowns, though, to the all-time of our knowledge, the full bear on has not notwithstanding been assessed. However, the English and Usa studies relied on surrogate measures of vaccine uptake; number of vaccines delivered/ordered (without a corresponding denominator) [11,xv] and the Singaporean study used convenience sampling with multiple assumptions for missing information [14]. Longer-term data were available from the KwaZulu-Natal Province of South Africa [13] and Sindh Province of Pakistan [12], which appeared to show some recovery afterwards an initial autumn in uptake; nevertheless, in Pakistan, part of the lockdown restrictions involved shutting downwards of outreach immunisation programme. The overall impact of lockdown on immunisation uptake in college-income countries, which maintained their routine immunisation programmes, is unclear.

Given the prolonged and repeated periods of lockdown, it is important to evaluate the overall effect on childhood immunisation uptake. The aim of this study was, therefore, to provide a longer perspective than previous studies by describing the pattern of childhood immunisation uptake in Scotland and England before, during, and immediately after the offset national lockdown implemented in response to the pandemic (23 March to 31 July), with comparisons to baseline data from 2019, by geographical area and socioeconomic impecuniousness.

Methods

Study design

This observational study took advantage of the natural experiment afforded by the COVID-19 pandemic and used routinely collected information for the year prior to the pandemic (2019) and immediately before, during, and after the first catamenia of "lockdown" imposed by the U.k. and Scottish governments in 2020. Information were available for Scotland and England; however, as discussed beneath, variations in time points at which the data were collected precluded direct comparisons. Of note, this analysis relates to the first national lockdown, which began on 23 March 2020, with restrictions easing gradually from over June and July 2020. The prespecified analysis plan is included within the Supporting information (S1 File). Pocket-sized changes were made to the planned visualisation format of the data (from bar to line plots) to amend illustrate the findings.

The vaccines chosen as indicators of preschool immunisation uptake were the hexavalent DTaP/IPV/Hib/HepB vaccine, (referred to here as "6-in-i"), which protects against diphtheria, tetanus, pertussis, polio, Haemophilus influenzae type b, and hepatitis B, and the measles, mumps, and rubella vaccine (referred to every bit "MMR"). In the UK, the 6-in-1 vaccine is recommended at age 8 ("commencement dose vi-in-1"), 12 ("second dose half-dozen-in-1"), and 16 ("third dose six-in-1") weeks of historic period, and MMR is given at 12 months ("first dose MMR") and 3 years 4 months ("second dose MMR") [16]. Uptake of the additional immunisations offered at the aforementioned ages (Meningococcal C, Rotavirus, and Pneumococcal) were not assessed.

For Scotland, we chose to primarily examine uptake within iv weeks of eligibility as this represents timely uptake of vaccinations every bit per the recommended United kingdom schedule [16] leading to the child being protected at the earliest recommended opportunity. All children living in Scotland who became eligible by age for any of the preschool immunisations of interest from January 2019 upwards to and including the week kickoff 28 September 2020 were included. Of secondary interest, and to allow descriptive comparisons with data from England, nosotros also analysed uptake at approximately 6 months (range 24 to 32 weeks) for the 6-in-1 and sixteen months for the first dose MMR. For England, equivalent data on uptake within 4 weeks were not available; therefore, the assay was conducted on uptake by 6 (six-in-1) or 18 months of age (first MMR), and monthly, rather than weekly, information were used.

Vaccine uptake was analysed in the following iv time periods: 1 January to 31 December 2019 ("2019"), 1 Jan to week offset 16 March 2020 ("prelockdown"), 23 March to week offset 27 July ("lockdown") and week offset 3 Baronial to week beginning 28 September 2020 inclusive ("postlockdown"). These fourth dimension periods were called to correspond with the beginning of the starting time Britain-wide lockdown equally announced past the UK government on 23 March 2020 [ane]. The end of the lockdown period is less well defined and varied both in approach and timescale between Scotland and England [17,18]. Broadly speaking, by the stop of July 2020, there was a substantial reduction in "lockdown" restrictions in both countries with the opening of many nonessential businesses and limited indoor meeting between households permitted; therefore, a pragmatic approach was taken to define the lockdown menses equally 23 March 2020 until 31 July 2020. Children were included in the time period at which they offset became eligible by age. As data from England were bachelor by month only, the prelockdown catamenia included January to end of March 2020.

Data sources

The Scottish data used in this newspaper were extracted in January 2021 from the PHS "COVID19 wider impacts on the health care system" dashboard, which is publicly accessible at https://scotland.shinyapps.io/phs-covid-wider-impact/. The dashboard includes aggregate information on immunisation uptake, including by the geographical area in which the child is living and the respective Scottish Index of Multiple Deprivation (SIMD) (both assigned based on the child's postcode registered on the Scottish national vaccination call-recall system, SIRS). The SIMD breaks Scotland into 6,976 small areas of similar population size and assigns i of five SIMD quintiles based on indicators of impecuniousness including income, education, and housing, with 1 representing the most deprived areas and 5, the least [nineteen]. We defined geographical areas by the Health and Social Care Partnership (HSCP) in which the child lives. Inside Scotland, there are 31 HSCPs that provide integrated health and social care to their population. Additional information on inclusion and exclusion criteria can exist institute in S2 File.

English data were extracted from the ImmForm arrangement, for January 2019 (representing the first extract for prelockdown period) to September 2020 (representing the final extract for postlockdown flow), which automatically receives monthly aggregate data on vaccine uptake from 92% to 95% of English language GP practices, provided by GP System Suppliers. These information are validated and analysed past Public Health England to check completeness, query any anomalous results, and are used to draw epidemiological trends, as well equally being used directly locally by the NHS for performance management. Information were available for immunisation uptake at age 6 months (each dose of the 6-in-1 immunisation) and 18 months (starting time MMR) just.

Statistical methods

The primary result examined was the change in percent uptake, inside iv weeks of eligibility, of each of the immunisations of interest betwixt baseline uptake rates in 2019 and during the lockdown catamenia for Scotland as a whole and past geographical areas or level of deprivation. Of secondary involvement were comparisons between 2019 and the other fourth dimension points listed above. Broadly comparable analyses were conducted to examine the primary outcome for England as a whole. Due to differences in data drove methods and historic period of kid at data extraction betoken, comparisons between Scottish and English information were descriptive only.

To compare uptake rates between time periods, amass binary logistic regression modelling was conducted, using vaccination status (vaccinated versus unvaccinated) as the dependent variable, and fourth dimension period as the explanatory variable. Separate analyses were carried out for each vaccine and country. When comparing HSCP or deprivation, an boosted interaction with HSPC or SIMD quintile was included in the model. Odds ratios (ORs) with 95% confidence intervals (CIs) were calculated for uptake in the period of interest compared to the 2019 baseline. Given the nature of the aggregated data bachelor, no adjusting for potential confounders or outcome modifiers was possible. Further methodological details tin can be establish in S2 File.

All analyses and generation of figures were performed using R/R Studio (4.0.3). All lawmaking is publicly bachelor via the EAVE II GitHub page (https://github.com/EAVE-Ii). Scottish data can exist accessed via the PHS wider impacts dashboard https://scotland.shinyapps.io/phs-covid-wider-impact/. The English language data used are included in the Supporting data, and whatever further queries should be directed to EarlyChildhoodBaseline@phe.gov.uk.

Ethics and funding

Ethical approval for this specific report was not required as we have used publicly available, anonymised, aggregated data. This report is reported as per the REporting of studies Conducted using Observational Routinely collected Information (RECORD) guideline (S3 File) [20]. No specific funding was received for this project; RM is funded by the Health Data Research Great britain Exhale hub.

Results

Information were available for the outcome of 439,754 vaccine invitations in Scotland and 4.08 million for England across all fourth dimension periods. Every bit many infants or children would be eligible for multiple immunisations during the study, these figures do non represent individual participant numbers. Detailed demographic data are not routinely collected and were therefore not available. For context, S1 Table shows population data from the relevant national records offices for births in Scotland and England by sex, maternal historic period, and maternal country of nascence from 2015 to 2020. It is expected that these information are broadly representative of the children included in this study.

All CIs presented are 95% CIs, and ORs are compared to the baseline year 2019 unless otherwise stated.

Preschool immunisation uptake increased during the lockdown period in Scotland

Across Scotland, the percentage of preschool children receiving their immunisations within 4 weeks of becoming eligible increased during the lockdown period for all 5 immunisations (Fig 1, Table 1, S2 Table). The change in percentage uptake compared to the 2019 baseline ranged from 1.iii% for the first dose 6-in-1 (OR 1.28, CI 1.eighteen to ane.39) to 14.3% for the second dose MMR (OR ane.8, CI i.74 to 1.87) (Table 1). Across all the immunisations visits, this equated to an boosted 7,508 preschool immunisations existence delivered in a timely manner over the lockdown period compared to the baseline rates of 2019. Uptake rates dipped immediately before the announcement of a national lockdown in mid-March 2020 (Fig 1), then peaked throughout June before starting to decrease. However, uptake remained significantly higher than 2019 during the postlockdown period (Fig 1, Table 1). Of annotation, prior to lockdown for both MMR doses, there was already a modest, increment in uptake compared to 2019 (Tabular array 1).

Fig 1. Percentage of children in Scotland immunised inside 4 weeks of eligibility.

(A) All doses six-in-1 vaccine; (B) MMR vaccine across Jan to September 2020 in Scotland. Lockdown period = blue shaded expanse. For January and February, a unmarried hateful monthly value is plotted, and from March onwards, weekly uptake is shown (see S2 Table for full data). Dashed horizontal lines (—) indicated the mean uptake in 2019 of the immunisation with the respective colour. The increase in uptake during the lockdown period was statistically significant (see Table 1 for details). MMR, measles, mumps, and rubella.

https://doi.org/10.1371/periodical.pmed.1003916.g001

Variation in uptake of preschool immunisations by geographical area

Baseline data from 2019 showed the pct uptake of preschool immunisations inside 4 weeks of eligibility varied widely past geographical HSCP and immunisation (Fig two, S1 Fig, S3 Table). In keeping with the rise in hateful uptake beyond Scotland for all vaccines, the percentage of children immunised in most HSCP increased betwixt 2019 and lockdown. All the same, non all followed this blueprint with a minority demonstrating a fall in uptake (Fig 2, S1 Fig, S3 Table). Care must exist taken when interpreting per centum results from the island HSCPs (Shetland Islands, Orkney Islands, and Western Isles) given the very small numbers of children involved (S3 Tabular array).

Fig 2. Percentage uptake by Scottish HSCP in 2019 and statistically pregnant increases between 2019 and "lockdown".

Left-hand side maps testify baseline mean pct uptake past HSCP in Scotland in 2019, and right-hand side maps evidence percentage point difference betwixt 2019 and lockdown for areas in which the deviation was statistically significant for each vaccine. Grey areas indicated HSCP where in that location were no statistically significant changes in uptake between 2019 and lockdown. Annotation that in Grampian, the second MMR dose is delivered at a later age; therefore, data for this surface area are recorded as "nonapplicable" (further details in S2 File). The full dataset can exist constitute in S3 Tabular array. Base layer map available from https://spatialdata.gov.scot/geonetwork/srv/eng/catalog.search;jsessionid=714BD98E15D22A8116824CA25B30DC02#/metadata/ac5e870f-8fc2-4c21-8b9c-3bd2311a583f, which contains public sector information licenced under the Open Government Licence v3.0. HSCP, Health and Social Care Partnership; LD, lockdown; MMR, measles, mumps, and rubella; Wks, weeks.

https://doi.org/10.1371/journal.pmed.1003916.g002

For individual HSCP, the statistical significance of the change in uptake varied by immunisation (Fig 2, S3 Table). Despite a general trend of improvement for the beginning half-dozen-in-one vaccine, we establish a significant change for only eight of the 31 HSCP, mainly centred around the more densely populated, urban key belt of Scotland (Glasgow City, Edinburgh, Stirling and Clackmannanshire, Due east Dunbartonshire, Falkirk, Fife, South Lanarkshire, South Ayrshire; Fig two). However, this design evolved with the dissimilar immunisation visits and with almost all HSCP showing a rise in uptake for both MMR immunisations, with percentage point increases every bit high as 30% (Angus, 74.1% versus 43.8%, OR 3.38,CI ii.61 to 4.37) (Fig 2, S3 Table).

Preschool immunisation uptake increased across all deprivation levels

Percentage uptake within 4 weeks of becoming eligible rose across all SIMD quintiles, between 2019 and lockdown, for all immunisations (Fig iii). The magnitude of this rise varied past quintile and vaccine (S2 Fig, S4 Table) from 0.3% (SIMD 4, commencement vi-in-1 dose, OR 1.one, 95% CI 0.9 to one.3) to 16.2% (SIMD v, second MMR dose, OR two.1, 95% CI one.9 to 2.3). The increase in uptake between 2019 and lockdown was statistically significant for all except starting time dose 6-in-one for the least deprived quintiles (four and 5) (S4 Tabular array). In the postlockdown menstruum, percentage uptake remained significantly higher than the 2019 baseline for all quintiles for each vaccine except for the first 6-in-i dose, in which only the most deprived quintile retained a significant increase (S2 Fig, S4 Table).

Fig 3. Mean percentage immunised by SIMD quintile in Scotland.

(A) six-in-1 vaccine; (B) MMR vaccine for Scotland. See S2 Fig and S4 Table for accented percentage ascension compared to 2019 and significance levels. LD, lockdown; MMR, measles, mumps, and rubella; PostLD, postlockdown; PreLD, prelockdown; SIMD, Scottish Index of Multiple Deprivation.

https://doi.org/10.1371/journal.pmed.1003916.g003

In keeping with previous observations [21], children in the least deprived quintiles were more likely to exist immunised and this relationship was broadly maintained throughout the study catamenia (Fig 3 and S3). While all quintiles improved uptake between 2019 and lockdown, whether the inequality between most and to the lowest degree deprived increased or decreased varied past vaccine type. For all doses of the vi-in-1 vaccine, in that location was a tendency to a convergent improvement, i.e., the gap in percentage uptake between the quintiles lessened, while for both MMR doses, at that place was further divergence in uptake rates betwixt virtually and least deprived (Fig iii, S4 Fig, S5 Table). The interaction of SIMD quintile and time period was nonsignificant for all 6-in-1 doses; that is to say all SIMD quintiles improved equally for this immunisation (S5 Table). However, for the first MMR dose, the improvement in uptake was statistically greater for SIMD quintiles 3 to 5 compared to SIMD 1, and for the 2nd MMR dose, SIMD 5 showed a significantly larger increase in uptake between 2019 and lockdown (S5 Table). This suggests that for the MMR immunisation, the factors leading to an improvement in uptake had greater positive affect for children living in less deprived areas.

"Grab-up" immunisation rates and comparison with data from England

Thus far, the Scottish data presented accept related to children receiving their immunisations as per the recommended schedule (inside iv weeks of the child condign eligible by age), representing a "gilded standard" in which the child is protected every bit early equally possible. It is recognised that some children will receive their immunisations afterward this point. This "catch-up" effect tin be seen in uptakes charge per unit for all Scottish children past the fourth dimension they reached between vi and eight months (vi-in-1), 16 months (first MMR), or 3 years 8 months (second MMR) (Fig 4A). Those becoming eligible during lockdown showed minimal alter in this longer-term mensurate of uptake for the iii doses of the 6-in-1 immunisation, a small increase in uptake of the showtime MMR, and a more than substantial increase in uptake of the second MMR (S6 Tabular array). These information suggest that while lockdown was associated with a beneficial effect on timely uptake of all infant and preschool immunisations, the bear upon on longer term or final achieved uptake was more variable, possibly reflecting a ceiling outcome on maximal uptake, for the earliest immunisations.

Fig 4. Percentage of children upwardly to date at 6/18 months in Scotland and England.

Overall mean pct of children immunised by approximately 6 months of age (all doses of half-dozen in1, meet y-axis for specific ages) or 16–xviii months (beginning MMR) for Scotland and England. Each bar contains children who became eligible for the immunisation of interest during the time catamenia indicated. (A) Scotland, (B) England *** p-value < 0.001, * p-value <0.05, ns, not significant. p-values calculated using binary logistic regression. LD, lockdown; MMR, measles, mumps, and rubella; PostLD, postlockdown; PreLD, prelockdown.

https://doi.org/ten.1371/journal.pmed.1003916.g004

For England, broadly equivalent data were available for children aged 6 months (all doses 6-in-1) and 18 months (get-go dose MMR) who had become eligible for their immunisations during the fourth dimension periods of interest (Fig 4B, S7 Table). These data demonstrated a small but statistically significant fall in uptake for all the immunisations in the lockdown periods compared to 2019, ranging from 0.5% (starting time dose 6-in-1, 95.viii% versus 96.3%, OR 0.89, CI 0.86 to 0.91) to ii.1% (third dose 6-in-one, 86.6% versus 88.seven, OR 0.82, CI 0.81 to 0.83) (S7 Table). Notwithstanding, much of the fall in uptake took place in the prelockdown period, specially for the tertiary dose 6-in-one, with a gradual recovery seen over the lockdown period itself (S4 Fig). A full general trend towards falling MMR uptake can too exist seen to predate the COVID-19 pandemic (S4 Fig).

Word

Nosotros found that early on uptake of infant and preschool immunisations (within iv weeks of a child becoming eligible) rose significantly for the duration of the start lockdown period in Scotland, resulting in thousands more children receiving their immunisations at the scheduled fourth dimension. Encouragingly, positive results were seen across all levels of deprivation, though some geographical variations were observed across Scotland. Improvement was also seen in longer term uptake of the first and second MMR immunisations (immunisation within four months of becoming eligible) in the lockdown menstruum. Findings in England differed, with a pocket-sized fall in longer-term uptake of immunisations observed for the lockdown period.

The Scottish data in particular claiming the early predictions of an adverse result of lockdown measures on childhood immunisation uptake and demonstrate the importance of continued surveillance throughout the various phases of pandemic command measures. From these information lonely, we are unable to fully determine what changes in both the barriers and motivators to vaccination may have led to this event; however, examining previous research can offering some suggestions. While the concept of vaccine hesitancy is a popular media topic, previous studies accept shown that the reasons given by parents for not vaccinating their children are frequently much more practical. A prepandemic report by the Royal Guild for Public Health in the UK found that the major barriers for parents who wanted to immunise their children were timing and availability of appointments and childcare duties [22]. For those who actively chose not to immunise their children, fear of side furnishings was a primal business and the negative effects of social media are increasing [22]. The lockdown has had a major effect on parental working patterns with almost ix 1000000 United kingdom employees furloughed and millions more working from dwelling house, frequently with the additional tasks of managing childcare as schools and nurseries were closed [23]. While this had made life significantly more challenging for many, more flexible working patterns may have made attending immunisation appointments easier for some.

Jarchow-MacDonald and colleagues [24] from NHS Lothian (which consists of HSCPs Edinburgh, West Lothian, East Lothian, and Midlothian) have suggested that ensuring the accessibility of immunisation centres, either by public ship or by providing mobile services to shielding families, was important in maintaining uptake during the pandemic, as was direct communicating with families with a preappointment phone call and reminder postcards. This gave families an opportunity to discuss the immunisation with a healthcare professional, a strategy that has been showed to exist of import in addressing parental concerns [25]. In fact, the reminder alone may have been sufficient to encourage parents to attend the first appointment [26]. The clear commitment of the Scottish Government to maintain the immunisation programme was also felt to exist an important factor [24].

In England, Bell and colleagues [27] conducted a large-calibration online survey of parents of children under the age of 18 months to assess their experiences of accessing immunisations during the early part of the UK lockdown (nineteen Apr to eleven May 2020). They highlighted the uncertainty of some families about whether the immunisation service was continuing, particularly amid non-white ethnic groups. While most felt information technology was important that their kid was immunised on time, Bell and colleagues reported that many parents felt the risk of catching a vaccine-preventable communicable diseases was reduced due to limited mixing with others. This suggests that an enhanced appreciation of the utility of immunisation was not a major motivator for parents to ensure they attended the immunisation appointments. These issues may well be reflected in the fall in immunisation uptake in England during the earlier part of lockdown reported here, and a delay in receiving the first dose vi-in-i may well led to delays in subsequent doses, meaning that the infants were unable to "catch upwards" by 6 months of age.

Other factors, which may take had an impact on promoting timely immunisation uptake, could include a reduction in fever, coughing, and colds, which may otherwise have caused parents to filibuster immunisations. Though specific data on this indicate are lacking, a meaning fall in the detection of Rhinovirus in adults was observed in 2020 compared to 2019 [28], suggesting that "normal" childhood respiratory infections are likely to take decreased. More piece of work is required to fully dissect the key factors in improving timely preschool immunisation uptake in Scotland. Clarity and publicity about the continuation of the immunisation programmes, telephone reminders, and the opportunity to hash out with healthcare professions seem likely to have had the most impact. We plan to use the data generated in this study to inform future work investigating these factors, including geographical differences and the introduction of policies such as reminders and publicity campaigns.

It is important to acknowledge the limitations of the data presented, many of which arise from opportunistically using routinely nerveless data rather than that obtained from a specific study blueprint. The SIRS electronic organization is well established and captures data on the entire kid population in Scotland. However, the aggregate surveillance data derived from the system that we could access lacked detailed data on several potentially important factors, not least of which was ethnicity, which is known to affect both immunisation uptake and attitudes towards immunisation. [29]. As shown in S1 Table, the proportion of mothers born exterior the UK is relatively low in Scotland (16.3% to 17.vii% between 2015 and 2020) and is almost one-half that of England (28.iv% to thirty.two%). It may non be advisable to extrapolate these information to countries with a significantly different ethnic makeup, and it is plausible that some of the deviation seen between the Scottish and English language information could be due to these factors.

In using the mean pct of the entire year 2019 as our baseline comparator, nosotros potentially run the risk of disruptive normal seasonal variation in immunisation uptake with the impact of lockdown measures. Ideally, straight weekly or monthly comparisons would be made between 2019 and 2020, though these data are not available. The enhanced detail and frequency of collection of immunisation uptake data and rapid dissemination (through the COVID dashboard) was in response to the pandemic and therefore just began in March 2020. However, quarterly trends published for previous years including 2019 exercise non prove major difference in uptake throughout the yr and in fact show a gradual decline in uptake yr on twelvemonth since 2015 [30]. In add-on, it is possible that 2020 uptake rates accept been underestimated, due to a lag in data entry into SIRS, which would particularly affect the "grab-up" rates (Fig 4A).

Therefore, caution must be taken not to overinterpret the results presented hither or extrapolate to significantly dissimilar populations with varying baseline immunisation uptakes rates and less robust immunisation programmes, the organisation of which may have been adversely affected by the pandemic. Even so, this written report has efficiently and quickly produced useful and valid results, which have the potential to aid the evolution of future inquiry and guide policy. The positive findings regarding immunisation uptake despite the extreme circumstances of the COVID-19 pandemic and associated lockdowns (in Scotland at least) is an important message to transport to back up public and professional person confidence in the preschool immunisation program and help normalise timely immunisation uptake for both parents and wellness services. Improving public and professional confidence is peculiarly vital given the current importance of promoting vaccination against SARS-CoV-2. Despite these encouraging data, it is not possible to ascertain from the numbers alone, which are the key contributing factors to improving uptake. This is a primal avenue of future research as lessons learnt can so be taken forward to optimise future immunisation programmes, both inside the pandemic setting and beyond. In addition, we have not yet assessed the potential impact of improved early immunisation uptake on rates of vaccine preventable diseases. Any observed changes in vaccine-preventable diseases (for example, pertussis in young babies) would be heavily confounded by the changes in behaviour such every bit social distancing and isolation for symptoms such as cough. Nonetheless, of the 5 vaccinations, at that place did appear to be an increase in overall coverage for the second MMR; therefore, monitoring trends in measles cases as we motion fully out of COVID-related restrictions may be of interest, though we would not exist able to infer causation.

The ongoing COVID-xix pandemic continues to stretch health services and adversely affect all areas of life, with children disproportionately bearing the burden of the indirect consequences of pandemic command measures such as the closure of schools and express social contact. Still, opportunities have also been created in terms of enhanced surveillance of wellness programmes. In this report, we have used such information to investigate the effect of the pandemic on infant and preschool immunisation uptake. Nosotros have demonstrated that a robust kid immunisation service can continue to evangelize high and even increasing uptake rates. Families will answer despite the many difficulties they confront, to ensure that children continue to exist protected again vaccine-preventable diseases. The challenge now is to use and expand on this knowledge to promote hereafter vaccination programmes, including those targeting SARS-CoV-two.

Supporting information

S1 Fig.

Per centum uptake past Scottish HSCP for 2019 (pale orange) and LD (dark orangish) with HSCP ordered by uptake for 2019 (note: this varies by immunisation). Dashed horizontal lines indicated the mean uptake for all of Scotland for the fourth dimension period of the corresponding colour. HSCP, Health and Social Care Partnership; LD, lockdown.

https://doi.org/10.1371/periodical.pmed.1003916.s001

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S2 Fig.

Absolute percentage change in uptake in Scotland compared to 2019 for each immunisations and SIMD for each time flow (A = Pre LD, B = LD, C = Post LD). Significance rates varied by immunisation and SIMD; for details, run across S3 Table. LD, lockdown; Post LD, postlockdown; Pre LD, prelockdown; SIMD, Scottish Alphabetize of Multiple Deprivation.

https://doi.org/10.1371/journal.pmed.1003916.s002

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S3 Fig.

Combined OR plot with 95% CI comparison each SIMD quintile (ii–5) to SIMD 1-most deprived for 2019 (dark bluish) and LD (light blue). Data for Scotland only. CI, confidence interval; LD, lockdown; OR, odds ratio; SIMD, Scottish Index of Multiple Deprivation.

https://doi.org/x.1371/journal.pmed.1003916.s003

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S4 Fig. Pct of children in England immunised by 6 months of age (first, 2d, and third dose half-dozen-in-ane) or 18 months of historic period (first dose MMR) from January 2019 to September 2020.

The starting time and end of the lockdown period is indicated by the majestic shaded surface area. MMR, measles, mumps, and rubella.

https://doi.org/x.1371/journal.pmed.1003916.s004

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S1 Table. Summary statistics for all alive births in Scotland and England 2015–2020 from the National Records of Scotland (Scotland) and Office of National Statistics (England).

Notation this tabular array gives an overview of the population as these data were non available for the individuals within the study. The engagement range encompasses the oldest to youngest children potentially included. For instance, those born in 2015 would be eligible for the second dose MMR in 2019 and those born in early August 2020 would be eligible for the offset dose 6-in-one during the "postlockdown" time menses. All the same, this does non account for children who may take migrated into/out of the areas since birth. Percentages are rounded to 1 decimal identify. MMR, measles, mumps, and rubella.

https://doi.org/10.1371/periodical.pmed.1003916.s005

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S3 Table.

A-E: Percentage uptake, percent point alter in uptake compared to 2019 and significance level for this change for each HSCP at each time menses. Each table shows results for a different immunisation. p-Values calculated using aggregate binary logistic regression and rounded to two decimal places. Results were considered pregnant if p-value <0.05 and 95% CI did not include one. Statistically meaning p-values are shaded light-green, and significant results for the 2019–LD comparisons are plotted on Fig two. CI, conviction interval; HSCP, Health and Social Care Partnership; LD, lockdown; NA, not applicable; OR, odds ratio; PostLD, postlockdown; PreLD, pre lockdown.

https://doi.org/10.1371/periodical.pmed.1003916.s007

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S4 Tabular array. Uptake of preschool immunisations by fourth dimension menstruum and SIMD and percentage betoken change in uptake compared to baseline 2019.

OR and 95% CI shown are for change in uptake compared to 2019. p-Values calculated using aggregate binary logistic regression and rounded to ii decimal places. Statistically pregnant alter in uptake compared to 2019 are shaded greenish. CI, conviction interval; LD, lockdown, NA, not applicative; OR, odds ratio; SIMD, Scottish Index of Multiple Deprivation.

https://doi.org/10.1371/periodical.pmed.1003916.s008

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S5 Tabular array. To assess whether the differences between change in uptake were statistically significant between SIMD quintiles, the interaction between time period and SIMD quintile was added into the model.

The baseline comparisons showed are for fourth dimension catamenia 2019 and deprivation quintile SIMD 1. If the 95% CI did not include 1, the interaction of time catamenia and SIMD was considered statistically significant, that is; there was a significant difference in the level of change (2019- time period) between the deprivation quintile and SIMD 1. For example, the increase in uptake during lockdown for SIMD 5 was statistically greater than the increment in uptake for SIMD 1. The ROR can exist used to summate the OR for uptake compared to the baseline levels past multiplying the ROR with the relevant OR in S3 table. p-Values calculated using aggregate binary logistic regression and rounded to two decimal places. CI, confidence interval; LD, lockdown; ns, non statistically significant (coloured green), interaction was statistically pregnant; OR, odds ratio; ROR, ratio of odds ratio, calculated by taking the exponential part of the coefficient of the interaction term from the interaction model; SIMD, Scottish Alphabetize of Multiple Deprivation.

https://doi.org/10.1371/journal.pmed.1003916.s009

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S6 Table. Scotland.

Uptake of preschool immunisations at an older age by time catamenia and point percentage change from 2019 with OR and 95% CI compared to baseline of 2019. Children are categorised into the time menstruum at which they became eligible for the immunisation as before and uptake data were extracted at a after stage when they reached the ages indicated in the immunisation cavalcade. Statistically significant changes are coloured green. p-Values calculated using amass binary logistic regression and rounded to two decimal places. CI, confidence interval; LD, lockdown; NA, not applicable; OR, odds ratio.

https://doi.org/10.1371/journal.pmed.1003916.s010

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S7 Table. England.

Uptake of preschool immunisations at an older age by fourth dimension period and point percent change from 2019 with OR and 95% CI compared to baseline of 2019. Children are categorised into the time period at which they became eligible for the immunisation as before and uptake data were extracted at a later stage when they reached the ages indicated in the immunisation cavalcade. Statistically pregnant changes are coloured green. p-Values calculated using aggregate binary logistic regression and rounded to 2 decimal places. CI, conviction interval; LD, lockdown; NA, not applicative; OR, odds ratio.

https://doi.org/10.1371/journal.pmed.1003916.s011

(DOCX)

Acknowledgments

Nosotros give thanks Public Wellness Scotland for making the data publicly available and acknowledge the back up of the HDR UK Exhale Hub and EAVE 2 collaborators.

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