“We don’t routinely check vaccination background in adults”: a national qualitative study of barriers and facilitators to vaccine delivery and uptake in adult migrants through UK primary care

Objectives Explore primary care professionals’ views around barriers/facilitators to catch-up vaccination in adult migrants (foreign-born; over 18 years of age) with incomplete/uncertain vaccination status and for routine vaccines to inform development of interventions to improve vaccine uptake and coverage. Design Qualitative interview study with purposive sampling and thematic analysis. Setting UK primary care. Participants 64 primary care professionals (PCPs): 48 clinical-staff including general practitioners, practice nurses and healthcare assistants; 16 administrative-staff including practice managers and receptionists (mean age 45 years; 84.4% women; a range of ethnicities). Results Participants highlighted direct and indirect barriers to catch-up vaccines in adult migrants who may have missed vaccines as children, missed boosters and not be aligned with the UK’s vaccine schedule, from both personal and service-delivery levels, with themes including: lack of training and knowledge of guidance among staff; unclear or incomplete vaccine records; and lack of incentivisation (including financial) and dedicated time and care pathways. Adult migrants were reported as being excluded from many vaccination initiatives, most of which focus exclusively on children. Where delivery models existed, they were diverse and fragmented, but included a combination of opportunistic and proactive programmes. PCPs noted that migrants expressed to them a range of views around vaccines, from positivity to uncertainty, to refusal, with specific nationality groups reported as more hesitant about specific vaccines, including measles, mumps and rubella (MMR). Conclusions WHO’s new Immunization Agenda 2030 calls for greater focus to be placed on delivering vaccination across the life course, targeting underimmunised groups for catch-up vaccination at any age, and UK primary care services therefore have a key role. Vaccine uptake in adult migrants could be improved through implementing new financial incentives or inclusion of adult migrant vaccination targets in Quality Outcomes Framework, strengthening care pathways and training and working directly with local community-groups to improve understanding around the benefits of vaccination at all ages.


INTRODUCTION
Adult migrants in Europe-particularly those from low-income and middle-income countries-may be at risk of underimmunisation for routine vaccinations due to missed vaccines and doses as children (due to lack of availability, war/disruption, poorly functioning health systems, and personal, social and physical barriers to accessing vaccines), and/or missed boosters, and differing vaccination schedules in their home country (especially for newer vaccines such as human

STRENGTHS AND LIMITATIONS OF THIS STUDY
⇒ A key strength of this study is the number and variety of primary care staff included from across England in diverse settings. ⇒ Interviewees were a self-selecting group, which may have affected the profile of those responding-a common consideration in qualitative research. ⇒ A large number of practices were involved, however, and this diversity and the scale of the study is likely to have added to the breadth of experience and solutions reflected in our findings, as well as enhancing the validity. ⇒ The structure and experience of primary care across Europe and between the devolved nations of the UK may differ so the recruitment only within England may limit the generalisability of the findings, however we note other European and international studies have come to the similar conclusions.
Open access papillomavirus vaccine (HPV)), and so may not be aligned with the UK's vaccination schedule on arrival. [1][2][3] Additional vaccines may be recommended if they return to their home country, or for specific occupations (eg, tetanus and hepatitis B). Some migrant populations are known to be at risk of underimmunisation 2 4-6 and were involved in recent outbreaks of vaccine-preventable diseases in Europe, including measles. 1 However, adolescent and adult migrants, beyond school age, are often not routinely incorporated into vaccination programmes on arrival to most European countries, including the UK. 7 The COVID-19 pandemic has highlighted shortfalls in engaging older migrants, and other marginalised groups, in vaccination programmes, 8 yet it has also presented a range of new opportunities and innovations in vaccine service delivery and policymaking to these groups, which merit greater consideration beyond the pandemic. The WHO's new Immunization Agenda 2030 (IA2030) 9 aims to improve vaccine coverage for vaccinepreventable diseases (VPDs), placing an emphasis on achieving equitable access for vulnerable populations and integrating catch-up vaccination for missed vaccines and doses throughout the life course. WHO recommends that all countries have a catch-up vaccination policy and catch-up vaccination schedule in place, to close immunisation gaps that would otherwise compound as populations increase in age, 10 11 and that it is always 'better to vaccinate late than never'. Although age limits apply for administration of a small number of vaccines, for most VPDs, providing vaccines late will still result in protection against morbidity and mortality, as well as reducing transmission and risk of outbreaks, with personal and community-level benefits. Specific WHO guidance for catch-up vaccination is available 10 ; in Europe, the European Centre for Disease Prevention and Control has published guidance on catch-up vaccination in children and adult migrants on arrival, 12 13 calling for healthcare providers to consider revaccinating adult migrants with uncertain vaccination status or no recorded history of vaccination. For UK arrivals, advice is available from the UK Health Security Agency (UKHSA) on the 'vaccination of individuals with uncertain or incomplete immunisation status' (see box 1), which will be relevant to most arriving migrants. 14 However, the extent to which these guidelines and policies are put into practice and prioritised by UK primary care-tasked with delivering the majority of the UK's vaccine programmes-is not known. No studies to date have explored the views and experiences of frontline primary care teams on approaches to catch-up adult vaccination in arriving migrants. We therefore did a national qualitative in-depth interview study with a range of primary care professionals (PCPs) to understand the challenges and needs of migrant populations with regards to catch-up vaccinations programmes, and facilitators and solutions to addressing gaps in service provision.

METHODS Design
Qualitative semi-structured interviews of both clinical and administrative staff were undertaken by telephone, following a topic guide collaboratively developed by the research team with support from a board of migrant representatives. The guide was piloted prior to data collection and iteratively developed throughout the data collection process, with the addition of further prompts and probes to develop richer understanding and addressed key areas around approach to vaccination of adult migrants, factors affecting vaccine hesitancy and uptake and possible interventions to strengthen delivery (box 2). The team comprised two general practitioners (GPs) and four academics, and was supported by a wider project board of a diverse group of migrant ambassadors. The range of professional and personal experience supported integration of multiple perspectives throughout the design, collection and analysis stages. The inclusion of two GPs in the research team brought knowledge of UK primary care to the study but required careful reflection during interviews and data analysis and was balanced by the inclusion of non-GP research team members at the interview stage.

Patient and public involvement
A board of migrant representatives supported the design of this study and development of the topic guides.

Participants
Participants were purposively sampled to capture the diversity of experiences in general practice, from administrative and clinical primary care roles and practices which varied both in size, and urban/rural location, factors which could influence the number of migrant patients and the organisation of care. Recruitment occurred via local CRNs, 'word of mouth' invitations from colleagues and a number of primary care newsletters, social media groups and practice manager mailing lists. All participants who expressed an interest in taking part were emailed a participant information sheet and consent form and invited to a telephone interview at a time of mutual convenience, with written informed consent being given in advance. Each participant was given £20 vouchers as compensation for their time.

Data collection
Telephone interviews, between 30 and 60 minutes, were carried out by JC (GP), FK (GP registrar) and AD and AFC (academic researchers) who made field notes in the majority of cases. Interviews were distributed randomly to research team members. Findings from the initial interviews were discussed across the group and led to the development of additional prompts and lines of questioning in the topic guide, as well as additional lines of questioning for non-clinical participants. All but three of the interviews were digitally recorded and transcribed verbatim by professional transcription service. The remaining three were lost through technical error but were typed up from extensive field notes. Transcripts were anonymised with a coded participant number and checked for accuracy. Data collection continued until there was thematic saturation 15 across all core themes as unanimously agreed across the team.

Data analysis
Data analysis was inductive, based on the stages of thematic analysis. 16 The transcripts were read repeatedly by AM (familiarisation) and emerging themes and patterns were identified and discussed with FK and JC who had also previously immersed themselves in the data. Initially, a coding of 10 transcripts on Microsoft Excel by AM allowed identification of emergent themes and discussion with FK and JC. NVivo (V.13) was then used to organise codes and iteratively refine and develop the emerging coding framework through a process of constant comparison, with close attention paid to non-confirmatory cases which contradicted existing themes. The final coding and themes were conceptualised through recurrent discussion by AM, FK, JC and SH. Active reflexivity was attempted from the study's onset, and input from across the multidisciplinary team, with support from the migrant advisory board, facilitated robust discussion throughout.

RESULTS
In total, 64 interviews were conducted. Forty-eight interviews were held with primary care staff: 25 GPs, 15 practice nurses, 7 healthcare assistants (HCAs), 1 clinical pharmacist, 11 practice managers and 5 receptionists. Participants were aged between 25 and 74 with a mean age of 45 years old (SD 11.8) and had been working in primary care between 1 and 35 years (mean 12.27 years SD 9.45). The majority of staff (50 (78.1%)) worked in Participants had varied exposure of vaccine delivery in migrant patients, but the data were convergent across this breadth of migrant healthcare experience, geographical area and participant profession. The main themes that emerged from data analysis were; the existence of multiple barriers to the delivery of catch-up vaccination to migrant patients, including vaccine acceptance and PCP training; the fragmented nature of adult migrant catch-up vaccination models despite existence of guidelines; the role of travel vaccination and occupational health have in adult migrant catch-up vaccination and next steps for strengthening delivery of catch up vaccination with existence of positive attitudes to strengthening primary care's role through numerous PCP enacted or suggested solutions to barriers given.

Existence of multiple barriers reported by PCPs to vaccine uptake in adult migrants
Patient acceptance of vaccines from PCPs Participants reported that their migrant patients express a range of views around vaccines from positivity to uncertainty, to refusal. Generalised mistrust and misinformation about vaccinations in migrant groups was commonly reported, which was often perceived by PCPs as resistance to information-sharing about the vaccine in question.
It's really hard to break through that barrier of… this is the evidence [about this vaccine]… I don't think they're listening… they're thinking… this is someone from my community saying this [other information]. And you're not from my community… I don't know if you have the best interests [in mind]. GP10

Different nationalities have different views on vaccines
Some PCPs gave their views on vaccine acceptance and uptake linked to specific nationalities, and most often reported beliefs or experiences that migrants originating from Eastern Europe, France and Italy, and Somalia and Bangladesh tend to be hesitant about vaccines. Table 2 provides illustrative quotes. Fixed negative views around vaccines were most often reported from Eastern European migrants, who were also viewed as having poor vaccination records and as wanting to follow a different vaccination schedule (as per protocols in their home country), with some returning to their own countries to be vaccinated. The doctor-patient relationship was highlighted Table 2 Perceptions of staff around acceptance and uptake in specific nationality groups

Participant reporting Quote
GP '…now it's more Bangladeshi, so Somalian was really with the MMR thing. But we still find more Bangladeshi families delaying or refusing the immunisation of their babies……So, yes they always blame… This is too much, the baby is young, we're not sure about the long term effects.' GP '[The Somalian population]…is a massive concern for us, with regards the patients unfortunately, falsely attributing MMR with an autism link……. I think it was the belief of autism, but why more in the Somali community than any other minority group, I'm not too sure.'  Open access as a key factor in tackling mistrust and vaccine hesitancy; some PCPs felt this represented a barrier and that it was easier for migrant patients to connect with PCPs from their own communities. The above represent barriers across all vaccinations. There were barriers reported to specific vaccines in the UK schedule and these have been summarised by vaccine in table 3.

Language barriers
Fragmented models for vaccine delivery to adult migrants Almost all clinical staff reported the availability of good catch-up programmes for childhood vaccination among recently arrived migrants, with some practice nurses (PNs) specifically quoting the Public Health England Schedule for individuals with uncertain vaccination status. Incentivisation for under-5s vaccination included the QOF, and well-resourced systems to ensure children are not missed, including the vaccination record 'red book' and using recall systems to contact patients, such as sending reminder texts. By contrast, adult migrants were often reported as being excluded from vaccination initiatives. One GP stated that over 5's and adults are sometimes assumed to be 'up to date from the country they come from', and many staff, especially GPs and administrators, were not aware of any catch-up vaccination programmes for adult migrants.
We don't routinely check vaccination background in adults. GP 16 We do catch-up vaccinations for children and young adults who've missed their primary vaccinations, but in terms of adults or people who are arriving to the UK, no. Admin 6 Ad hoc. We haven't had a particular programme for [adult catch up vaccinations]. GP15 Where adult catch-up vaccination was provided, models of delivery were diverse and fragmented, comprising a Open access range of clinics and providers, different staff members (primarily nurses) and a combination of opportunistic and proactive programmes. Providers of catch-up vaccination for adult migrants included: NHS GP practices, detention centres (for undocumented migrants and asylum seekers), migrant-specific or language-specific clinics, private clinics and specialised clinics (eg, sexual health clinic in China Town), with distinct benefits and challenges.
Detention centres: Interpreters weren't always readily provided when I was at the detention centres. We found that really difficult and it took several visits [to determine which vaccines were required and these to be given]. PN13 [on local community infectious disease led clinic] And they have a large Somalian support network there, so they have interpreters, and bits and piec-es………. They will go in, and there will be a Somalian phlebotomist and doctor, and so they engage with it that way, much easier. HCA 6 Respondents reported vaccinations programmes were a mix of opportunistic and proactive delivery approaches. Proactive programmes included methods such as setting up searches, call and recall systems to contact patients and targeted campaigns for specific vaccinations (eg, influenza).
We run recalls [for adult migrant catch-up] constantly throughout the year. We will target separate cohorts of patients, just so we can make sure we're recalling everybody. Admin 5 Opportunistic usually meant identifying a patient needed a vaccination when they were attending the practice for another reasons. The vaccine could be given immediately, or the patient booked into an appointment at a later date.
…if I notice and if I remember or have time to mention it, then I encourage people to… [but] they're usually coming with quite a few issues, and we're using an interpreter… there's a lot to cover…[hence no time to cover vaccination]. GP 18 There are also diverse approaches to vaccine delivery between practices, with different staff involved in different aspects of the vaccine programme. However, many programmes are nurse-led, with the practice nurse having main responsibility.

Open access
[It's a] mixture of me, one of the partners, and then the reception staff are the ones who actually call the patients and arrange for them to come in. Admin 13 If they're struggling to get somebody to agree [to take a specific vaccine]… we get the named GP. to take responsibility for having that conversation and trying to talk them round. Admin 9 …our vaccines are really well-run at the practice by one of the nurses in particular. She runs the whole immunisation program, the childrens, the flu, the catch up, everything. So, I would imagine that there's probably a lot going on that I'm not aware of. I suspect and she always goes on updates and is very much aware of new guidance to things so I'm sure that she's probably doing a lot of stuff behind the scenes that I'm not aware of. GP 3

Travel vaccination and occupational vaccines
Provision of catch-up vaccines and additional vaccines to adult migrants was also mentioned in the context of travel and occupational requirements. Delivery of travel vaccinations was highlighted by a variety of participants for migrants visiting their home countries and travelling to Haj.
I think people are very good at knowing they need vaccinations, especially people who have been settled in England for quite a long time and are maybe making an infrequent return visit home to may visit relatives or family elders or to go for a celebration. Admin 6 They will go for the bare minimum of what is offered, or what they need to have as certificated. If they're doing the pilgrim to the Haj, then they have to get the meningitis. If they… need yellow fever, they'll get the yellow fever…or they just don't have anything. PN 2 Different nationalities were reported as having varying levels of engagement with travel vaccine uptake. One PN reported Bangladeshi families travelling more being 'more engaged' than Middle Eastern people. Another reported Europeans as 'more engaged with travel clinics than…people… from Pakistan, India, Bangladesh and African countries'. (PN2) African patients were described as having a poorer uptake of travel clinics than Europeans 'people returning to DRC or Tanzania…their uptake is poorer than younger European people' PN2.
Participants noted that travel clinics can also be an opportunity for opportunistic adult catch-up: The nurses who do the travel clinics are certainly very switched on to catch-up vaccines and will make sure everybody's up to date with DTP and MenACWY, even if they're not going to a country for which you need ACWY. GP 17 Travel vaccines were often given privately due to recommendations these should be done outside of the core GP contract, and this was primarily the case for adults but not children.
We do … Hepatitis A and then typhoid as part of the core contract. Anything else we direct patients to a private travel clinic. GP 24 However, there was variability in provision, with one GP stating: 'We don't charge for anything, including malaria pills' (GP 17). This would impact the 'migrant population who are going backwards and forwards to their home countries [and] constitute quite a large percentage of patients that we see for travel clinics' (GP 17).
Occupational vaccines were mentioned as sometimes being provided 'outside the schedule' for healthcare staff, such as nurses.
[Hepatitis B] vaccination is not within the schedule, so it has to be treated like a private prescription… some of them are nurses …[and they ] usually come from the South Indian population. Carers and nurses. GP 4 We shouldn't be seeing people wanting occupational health-related vaccination, but we do often get people asking for that. PN 1 Strengthening vaccine delivery in UK primary care Primary care staff raised a range of potential solutions and action points to increasing vaccine uptake, especially in adult migrants, including addressing personal, societal and physical barriers to vaccination systems through UK primary care alongside financial incentives to primary care to deliver adult catch-up vaccination. Key barriers and respective solutions identified by participants have been summarised in table 4.

DISCUSSION
Key findings WHO's new Immunization Agenda 2030 9 calls for greater focus to be placed on delivering vaccination across the life course, targeting underimmunised groups for catch-up vaccination at any age, with primary care services therefore having a key role to play in the UK context. In our study, however, participants highlighted direct and indirect barriers to delivering catch-up vaccines in adult migrants who may have missed vaccines as children, missed boosters and not be aligned with the UK's vaccine schedule. Barriers were noted at a personal and service-delivery level, with themes including: lack of training and knowledge of guidance around catch-up vaccination among staff; unclear or incomplete vaccine records; and lack of incentivisation (including financial reimbursement), prioritisation and dedicated time and care pathways. Adult migrants were therefore reported as being excluded from many vaccination initiatives, most of which focus exclusively on children. In addition, PCPs reported that migrant patients express a range of views around vaccines to them, from positivity to uncertainty, to Open access Improving uptake of catch-up vaccination in this group will require new care pathways and training of frontline staff, alongside working directly with local community groups to communicate the benefits of vaccination at all ages. In addition, greater collaboration across systems and community groups and culturally competent campaigns are warranted. At a time when COVID-19 vaccination programmes are being rolled-out across the world, this study adds important understanding regarding the specific vaccination needs and concerns of migrants, and the challenges faced by the staff delivering vaccination programmes to migrant populations and older cohorts.

Strengths and limitations
A key strength of the study is the number and variety of primary care staff included from across England in diverse settings. Interviewees were a self-selecting group, which may have affected the profile of those responding-a common consideration in qualitative research. However, a range of practices were involved, including those that do not see many migrants, and this diversity and the scale of the study is likely to have added to the breadth of experience and solutions reflected in our findings, as well as enhancing the validity. We noted that often participants made broad generalisations about specific nationality groups, which needs to be considered with commitment to equality, diversity and inclusion when assessing findings. The structure and experience of primary care across Europe and between the devolved nations of the UK may differ so the recruitment only within England may limit the generalisability of the findings, however other European and international studies 7 17 18 have come to the similar conclusions in terms of healthcare provider, system and patient-related barriers to catch-up vaccination in relation to adult migrants, so we feel that this would be unlikely.

Next steps for strengthening catch-up vaccination in older cohorts
We found a range of direct and indirect barriers to delivering catch-up vaccines in adult migrants who may have missed vaccines as children, missed boosters and not be aligned with the UK's vaccine schedule, from both a personal and service-delivery level. Our findings concur with those of similar study in Norway 17 which found no consistent or structured approach to vaccinating adult migrants in Norway, including no guidelines from governing bodies on how to organise vaccination to adult migrants. Reasons why adult vaccination is not prioritised included tuberculosis screening and treatment taking precedence, and a common assumption among healthcare providers that vaccinations are dealt with in childhood. 17 A questionnaire survey of experts across Europe, 7 and policy analysis, 19 found that policies and practice differ across European countries with respect to adult vaccination and the inclusion of migrants in vaccine systems on arrival. Only 13 of 32 countries in the European Union/European Economic Area (EU/EEA) had policies in place to offer MMR vaccines to adult migrants, with 10 countries reporting that they would charge fees. 7 Variations in vaccine policies targeting adult migrants were reported in another European survey. 20 In addition, it is well known that some migrants face a range of barriers to health systems more broadly. This suggests that more inclusive policies are required placing an emphasis on  Open access new approaches to ensure older migrants are included, and that such policies are well implemented in practice. Implementation will be key, and our study raised numerous points that merit greater consideration. Service delivery barriers have previously been described in other areas of migrant health, including screening for infection, with GPs citing concerns about lack of awareness around the health needs of migrants and insufficient time and resources. 21 22 It has previously been noted that negative biases from healthcare staff towards migrant patients or preconceptions about vaccine hesitancy in specific ethnic groups may have an impact on patient trust, 23 24 which is known to be a major factor in vaccine uptake. 25 Education and training of frontline providers will be a critical component given the critical role that the PCP-patient relationship has for building trust in vaccination. This must involve raising awareness of the diverse experiences of migrants and how to approach potential vaccination concerns with sensitivity, as well ensuring an understanding around the potential low vaccine coverage in their countries of origin as children, different dosing schedules and particularly low coverage for newer vaccines. For HPV, for example, global coverage for the final dose was only 13% in 2021 26 -suggesting many migrants aged under 25 years would be eligible for HPV vaccination as part of the UK's more advanced programme. However, likely a key factor will be financial incentivisation to encourage practices to target potentially underimmunised adults for catch-up vaccines, which was a recurrent theme among those interviewed. Catch-up vaccination could be considered at various entry points, for example, the New Patient Health Check or the NHS Health Check. Since April 2020, MMR now comes with an item of service payment, including for catch-up vaccination in patients who missed out on scheduled vaccines, which should encourage practices to offer appropriate vaccinations to patients regardless of age.
Tackling hesitancy and educating migrant and broader ethnic minority communities about the benefits of vaccination across the life course will also be a critical component, 22 27 with COVID-19 presenting numerous innovations in service delivery in this area that merit further consideration to routine vaccination going forward including outreach, policy shifts to facilitate registration of migrants with primary care providers and anonymous vaccination in trusted locations. 22 28 We found that certain nationality groups (Somali, Eastern Europeans and Bangladeshi) may be more hesitant to receive vaccines than others, or reluctant to receive certain vaccines, aligning with a recent systematic review that found nationality/country of origin to be a key determinant of vaccine uptake for routine vaccines and COVID-19 vaccines in European data sets. 8 In this study, acceptance barriers were mostly reported in Eastern European and Muslim migrants for HPV, measles and influenza vaccines, with 23 significant determinants of undervaccination in migrants found (p<0.05), including African origin, recent migration and being a refugee/asylum seeker. 8 A systematic review of interventions to improve vaccination uptake in newly-arrived migrants to the EU/EEA 29 highlighted the potential solutions of social mobilisation and outreach programmes, planned vaccinations and educational campaigns. Our data points to a recommendation for policymakers to include adult migrants especially in catch-up vaccination programmes on arrival, and to ensure policy around the delivery of catch-up vaccination across the life course is implemented in practice.