**4. Discussion**

Measles vaccination uptake in this cohort of children and young adults in Wales is reassuringly high, with coverage of one dose over 95% in all NHS-registered children aged 2 to 25 years. However, potential remains for outbreaks of measles where unvaccinated individuals are clustered. All routine childhood vaccinations in Wales should be recorded in the child health system until 16 years of age to manage appointment call and re-call and enable accurate reporting. However, we have seen that administrative records are not always correct, and reconciling multiple data systems may help improve accuracy. Despite high coverage, minor improvements in some age groups may be the difference between reaching the 95% coverage target or not. Although the oldest individuals in this analysis would have been scheduled for vaccination in the latter years of the decline in MMR uptake seen following the Wakefield scandal, coverage appears high. However, the young adults who were young children at the time of the negative publicity might explain some of the significantly reduced odds of vaccination in those aged 19 years and older. This analysis may also exclude a number of individuals who are not registered with the NHS, and therefore not included in the datasets used to produce these figures.

MMR coverage is frequently reported as a measure of the proportion of the population protected from measles infection. These analyses have identified that over 4000 single (or duel MR) antigen measles doses had been received by those in the study cohort. However, the receipt of non-MMR vaccines has decreased in younger age groups. Some of these records may be miscoded and validation of the type of vaccination received would be necessary to have accurate records of which viruses individuals are protected against.

A small proportion of the study population (0.7%) had a GP Read code indicating measles vaccine refusal. A higher proportion of those in younger age groups had a refusal code, which could be an indication of a recent increase in vaccine hesitancy. However, this trend could also be due to improvement in coding over time. Although this study tries to focus on factors associated with low coverage in those who have not actively refused vaccination, there is suggestion of variation in refusal by different characteristics, some of which, such as residing in rural areas, appear to be associated with refusal but not other reasons for being unvaccinated. Monitoring refusals would be beneficial to highlight any concerns or mistrust as early as possible [28]. The USA has seen a recent increase in exemptions for MMR vaccine due to religious, philosophical or personal reasons, which may be contributing to a resurgence in cases [29].

Excluding those with known refusal, we have seen that inequitable coverage is particularly prevalent in households with more children and for those born outside of the UK. Living in a deprived area, being eligible for free school meals, lower level of maternal education, and having a recorded language other than English or Welsh were also associated with lower coverage. These factors are similar to those mentioned in previously published literature [10,12,15,30]. Lower coverage persists in deprived urban areas, and factors relating to deprivation are complex and hard to separate out.

Evidence from this study is useful to develop tailored interventions; for example, community health care visits [31], which in this case could be prioritised for large households with multiple unvaccinated children, or joint scheduling for siblings that require catch-up. Having had previous vaccines meant there was a higher chance of having had measles-containing vaccine, suggesting it may be efficient for catch-up campaigns to target more than one vaccine programme. Improving accessibility of resources and using tailored public health messaging may reduce inequities [32]. In addition, using the WHO Tailoring Immunisation Programmes approach can help us understand specific barriers in communities identified as having lower coverage [33,34].

A recent review has suggested migrants are half as likely to be vaccinated compared to non-migrants [35]. Challenges specifically relating to migrants who have transited through a number of countries, and refugees, include lack of information on vaccination status at arrival, fear of registration with medical authorities and lack of coordination between public health authorities of neighbouring countries [36]. It is likely that recording of immunisations in those who were on vaccination schedules different to the UK is difficult and parents often do not have evidence of their child's previous vaccinations, which makes entering dates into the system, and scheduling further doses, challenging. UK guidance indicates restarting a vaccine course if vaccination history is uncertain [37]. Tailoring immunisation services to ensure there are no language barriers when carrying out vaccination status checks and ensuring flexible systems for recording immunisations from overseas could be beneficial. Low vaccination coverage in Eastern European communities has been linked to measles outbreaks in the UK, with language, literacy and trust of health care providers identified as potential barriers [38]. Building trusting relationships with minority groups such as Gypsies, Travellers and Roma may also improve utilisation of health care services including uptake of vaccination [39].

There are limitations to this study. Some individuals will not be registered with NHS health services, and those who do not have a NCCHD record were excluded, which will affect those who first resided in Wales after 16 years of age. Additionally, some vaccinations recorded in primary care GP data, but not on the NCCHD record, for older ages may be due to catch-up immunisations given more recently. There is the possibility of 'ghost records' for those who have moved away and not notified the system. The multivariable analysis was restricted to those without missing information, which disproportionately affected some groups. This analysis would exclude those families who moved to Wales since 2011 when the census took place, as variables such as mothers' highest education level were derived from census data only. The higher vaccine coverage and reduction in effects that were seen in the multivariable analysis may therefore be due to this restricted cohort only including those who have been settled in Wales for a longer time period. It is challenging to draw conclusions around those factors, which showed different associations in the univariable analyses when using the full and restricted study population, including comorbidities and mothers' age. Additionally, some data may not reflect the current status of an individual as it may be out of date. This includes information taken from the 2011 census and information on language, as even if a language other than English or Welsh

is recorded, a person could be bilingual or have sufficient understanding of English or Welsh to access services and make an informed decision around vaccination. However, this analysis is still a useful indicator to highlight areas at risk of outbreaks and where coverage could be improved. This is a large population study that has been able to provide new evidence on a number of characteristics associated with measles vaccination coverage in Wales.

Reducing inequalities in vaccination coverage remains key for preventing measles outbreaks and reaching the WHO measles elimination targets [1]. Disruption to routine vaccine schedules during the COVID-19 pandemic may have exacerbated the inequalities reported here, making the need for catch-up activities even more pressing [40]. Reported measles cases in Europe decreased from mid-2020 [41], but now that travel restrictions have been fully lifted, the likelihood of a resurgence in cases is high and identifying/reducing inequalities in vaccine coverage should remain a priority.

**Supplementary Materials:** The following supporting information can be downloaded at: https: //www.mdpi.com/article/10.3390/vaccines11030680/s1, Table S1: Uptake of one or two doses of measles-containing vaccine in those aged 4 to 25 years alive and resident in Wales as of 31 August 2021, without a vaccine refusal code, by individual characteristics. Univariable Odds Ratios and 95% Confidence Intervals are also presented. Groups with uptake under 95% are indicated with bold text. Analysis is presented for the whole study cohort.

**Author Contributions:** Conceptualization, M.P., S.C., M.B.G. and L.G.; methodology, M.P.; formal analysis, M.P.; data curation, M.P.; writing—original draft preparation, M.P.; writing—review and editing, M.P., S.C., M.B.G. and L.G.; visualization, M.P.; supervision, S.C., M.B.G. and L.G.; project administration, M.P. and S.C. All authors have read and agreed to the published version of the manuscript.

**Funding:** This research received no external funding.

**Institutional Review Board Statement:** Not applicable.

**Informed Consent Statement:** Not applicable.

**Data Availability Statement:** The data used in this study is available from the SAIL Databank at Swansea University, Swansea, UK, which is part of the national e-health records research infrastructure for Wales. All proposals to use SAIL data are subject to review by an independent Information Governance Review Panel (IGRP). Before any data can be accessed, approval must be given by the IGRP. The IGRP gives careful consideration to each project to ensure proper and appropriate use of SAIL data. When access has been approved, it is gained through a privacyprotecting safe haven and remote access system referred to as the SAIL Gateway. SAIL has established an application process to be followed by anyone who would like to access data via SAIL at: https://saildatabank.com/data/apply-to-work-with-the-data/ (accessed on 16 March 2023).

**Acknowledgments:** This work was led by M.P. as part of her PhD at Swansea University. The authors acknowledge members of the SAIL Databank who have made the data available for use in this project as well as all the immunisation teams across Wales who facilitate the recording and data quality of the vaccination data in the Wales Children and Young Persons Integrated System.

**Conflicts of Interest:** The authors declare no conflict of interest.

#### **References**


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