A systematic review of barriers and enablers associated with uptake of influenza vaccine among care home staff

Barriers and enablers to vaccination of care home (CH) staff should be identified in order to develop interventions to address them that increase uptake and protect residents. We aimed to synthesis the evidence describing the barriers and enablers that affect the influenza vaccination uptake of care home (CH) staff. Method: We searched


Introduction
Influenza infection is a serious health risk for older people due to their overall frailty, immune function deterioration, nutritional deficiencies [1], and the possibility of infection transfer from staff and visitors in care homes (CHs) [2]. In fact, more than 90 % of influenzaassociated deaths occur among older people [3], with influenza responsible for 2.5-8.1 % of deaths among those over 75 years old [4]. During the 2019/20 influenza season, Public Health England (PHE) reported 3,936 acute respiratory infections outbreaks with 69.9 % of them occurring in CHs [5]. Almost a quarter of these outbreaks were caused by influenza viruses [6]. Influenza outbreaks in CHs have been associated with an increased risk of hospitalization and death among residents, especially those with underlying health conditions. It has been estimated that influenza was responsible for a significant proportion of hospitalizations and deaths in CH residents, both with and without comorbid conditions [7][8].
During the winter season, a notable percentage of CH staff (ranging from 10 to 30 %) tend to be infected with influenza, which could potentially lead to the introduction of the virus in CHs [9,10], with nearly 50 % of infected staff still being contagious even when afebrile [11]. CH staff can be a source of infection and increase the risk of an influenza outbreak since many of them continue to work despite being infected [12]. This may be attributed to financial limitations, as many CH staff are dissatisfied with their compensation [13] and may not be able to afford taking time off work. CH staff are at high risk for influenza virus infection and act as a reservoir for the influenza virus, participating in the transmission of influenza to CHs [14].
Therefore, influenza vaccination is necessary for CH staff, as protection weakens and virus strains change on a regular basis [15]. The seasonal influenza vaccine has been proven effective and safe [16,17], and shown to be the best method currently available for reducing the consequences of influenza [18]. Health authorities and national organizations recommend influenza vaccination for individuals who provide care for those with medical conditions as a critical patient safety measure [19][20][21].
However, the influenza vaccination rate for healthcare workers (HCWs) is often below recommended levels in most countries [22,23], despite persistent recommendations and public health regulations on immunizations globally [24][25][26]. Notably, influenza vaccination rates for CH staff are lower than those in all other healthcare settings (e.g., hospitals) [24,[27][28][29][30], putting CH residents, who are vulnerable to influenza and its complications, at serious risk of infection.
The impact of CH staff's vaccination on reducing influenza among CH residents remains a controversial issue, primarily due to the limited availability of scientific evidence and the low quality of research studies [31]. While the existing evidence might not strongly support CH staff vaccination for protecting CH residents [32,33], there is also a lack of evidence against its effectiveness [34]. However, one review indicates that a higher influenza vaccination rate among CH staff reduces allcause mortality among CH residents [35], while also ensuring work stability by reducing staff sickness absence and related job interruption [36,37]. To help mitigate the risk of outbreaks and alleviate the associated burden, it is necessary to ensure that CH staff who provide assistance to elderly individuals receive vaccinations [38]. Furthermore, influenza vaccination has also been estimated to be a cost-effective preventative measure across a range of different health systems [39,40].
Many systematic reviews have explored determinants associated with epidemic and seasonal influenza vaccination in HCW population in general [41][42][43][44][45][46][47][48][49][50][51][52], but no reviews have been specific for CH staff. Identifying the barriers and enablers related to influenza vaccine uptake among workers in these settings is necessary to inform the design of an intervention since many factors differ from one health care setting to another.
To improve the influenza vaccination rate for CH staff, intervention design is recommended to be based on a theory to enhance the likelihood success of the intervention [45]. There are various theories focused on changing behaviour, many of which with overlapping constructs. The Theoretical Domains Framework (TDF) is a synthesis of 33 theories organised into 14 theoretical domains [53][54]. The TDF has been shown to be an effective tool for determining factors influencing behaviour, barriers to changing behaviour, and how internal and external factors influence individuals' decisions [55]. Additionally, the TDF is also linked to a taxonomy of behaviour change techniques, which can be used to develop interventions, as well as evaluating these interventions [56]. In this systematic review, we used the TDF as a lens through which to understand the barriers and enablers affecting the uptake of influenza vaccine among CH staff.

Aims and objective
To inform the design and development of a CH staff intervention to improve influenza vaccination uptake, the aim is to undertake a narrative synthesis of the literature to identify reported barriers and enablers and then to map them to the relevant domains of the TDF.

Search strategy
This systematic review was registered with the International Prospective Register of Systematic Reviews (PROSPERO: CRD42021248384). A scoping review was performed to inform the development of the search strategy, identify data extraction tools, select the quality assessment tools and establish inclusion and exclusion criteria.
We searched the following databases: PubMed Central, CINAHL (EBSCO), PsycINFO (EBSCO), AMED (EBSCO), MEDLINE (Ovid), EMBASE (Ovid), IBSS (International Bibliography of the Social Sciences), and Scopus in May 2021. The search was updated in February 2023 and one additional study included. A combination of subject heading and key words derived from the review question were used, such as "care home," "long term care facility," "staff," "influenza," "vaccination," "immunization," "barrier," "enabler," "knowledge" and "attitude". A detailed search strategy for PubMed (Appendix A) was developed and adapted for the other databases. The reference list of included articles and relevant systematic reviews were searched to elicit further articles. The search result was exported to EndNote and duplicates removed.

Inclusion and exclusion criteria
We included all primary studies explicitly reporting factors (barriers or enablers) that influence the influenza vaccine uptake among CH staff regardless of the research methodology and study design. We excluded studies not published in English as well as those where the vaccine concerned was not the seasonal influenza vaccine (e.g., Covid, H1N1). We included only studies that reported the results for CH staff separately. Reviews, conference abstracts and studies reporting only nonmodifiable determinants (e.g., age, gender, ethnicity) were excluded.

Study selection
Three steps were applied to identify the eligible studies. Firstly, following duplication removal, two independent authors (FA and AB) screened the titles of all studies identified in the search. Any disagreement during titles screening was resolved through discussion. Secondly, the abstracts of relevant or unclear titles were screened by the same authors. If there was disagreement during abstract screening or an abstract showed insufficient data, the full text was retrieved to assess its eligibility. Finally, the process of screening the full texts was divided among the authors (FA, MT, SC, AP) to identify eligible studies for inclusion in the review. The results of this process were compared and discussed among the team to ensure consistency and accuracy in the selection of eligible studies.

Data extraction
One reviewer (FA) extracted the following data: first author, titles, year of study, study objectives, study design (e.g., survey, interview), type of CH (e.g., nursing, residential), ownership of CH (e.g., for profit, public), number and size of CH that participated in the study, number of participants and response rate, vaccination rate and type of participants (e.g., nurses, nursing assistants). Barriers and enablers were also extracted from the studies and mapped to the TDF domains. To ensure the accuracy of the data extraction, a second reviewer (DW) checked a sample of 20 % of papers. If the study included data for other healthcare settings (e.g., hospitals), only data related to CH staff was extracted. The computer software program NVivo was used to facilitate the extraction and mapping of barriers and enablers.

Quality assessment
The Critical Appraisal Skill Program (CASP) [57] was applied for qualitative studies, whereas the Center for Evidence-based Management (CEBMa) [58] critical appraisal checklist was applied for cross-sectional studies. The quality assessment was carried out by one reviewer (FA), with a 20 % sample of studies assessed independently by a second reviewer (MT). Agreement was not directly measured, however, only small disagreements over the quality of the study existed and were addressed by discussion.

Data synthesis
One reviewer (FA), trained in the use of the TDF, mapped the barriers and enablers to relevant TDF domains. A behavioural scientist (SS) checked mapping for 20 % of the included studies. Any disagreement was resolved through discussion until consensus was reached. We reported the frequency of the TDF domains to provide a summary of the domains that were most frequently mentioned across studies. The data within each TDF domain were categorized into common patterns of barriers and enablers. Two reviewers (FA and MT) checked the agreement of the extracted data with the assigned categories and determined whether the data were appropriately allocated to barriers or enablers to influenza vaccine uptake.

Results of the search
The database search retrieved 6352 articles (Fig. 1). Following the removal of duplicate articles, a total of 3828 studies were excluded based on screening of their titles and abstracts. One hundred and ninetyseven studies were reviewed in full text. Of these, 155 studies were excluded and examples of reasons for exclusion are presented in Fig. 1. In total, 42 studies met our inclusion criteria. The level of agreement between the reviewers at titles, abstract and full text screening was 81.8 %, 89.9 % and 92 %, respectively, with Cohen's k 0.12, 0.71 and 0.83, respectively. No further studies identified from searching the reference

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list of the included studies and the relevant systematic reviews.

Quality assessment
The quality assessment of the quantitative studies is summarized in Table 2. Regarding the quantitative studies, most had a clear research question, used appropriate study design, and clearly described the method of subjects' selection. There is a range of questionnaire validity and reliability assessments across the included studies. One study examined content validity and internal consistency [88], while another utilized data from a pre-validated survey [69]. In two studies, the questionnaires were based on previously published questionnaires [91,92], whereas three studies utilized pre-tested questionnaires but did not report any information on their validity [93,97,98]. Additionally, eight studies included in the review reported conducting a sample size calculation and aimed to recruit all eligible participants [78,85,87,91,93,94,98,99]. There are concerns in terms of quality due to the possibility of selection bias, representativeness of the sample, and lack of pre-study calculation of statistical power. Such quality concerns can lead to a restricted judgment on whether a satisfactory response rate was achieved or not. Another concern relates to the lack of use of a validated and reliable survey instrument. Some studies lacked sufficient details because they were embedded within a larger study design.
The quality assessment of the qualitative studies is presented in Table 3. The qualitive content of four studies was part of interventional studies [59,64,67,68,100], whereas four studies used mixed-methods [78,87,90,91]. Therefore, the quality assessment was focused on the qualitative part of the studies. All studies explicitly stated the aim of the research. The qualitative methodology, the research design and data collection were appropriate for most of the included studies. Some studies described the recruitment strategy inadequately, failed to examine the relationship between the researcher and the participants, and did not address any potential bias during the formulation of the research questions and data collection process. Some studies described the ethical issues insufficiently and did not describe the method used for the analysis. Although some studies had a clear statement of the findings, these findings were authors' interpretations -without the use of participants' quotes-which may affect the credibility of the findings.

Barriers and enablers
During the data extraction phase, we identified a total of 691 barriers and enablers influencing influenza vaccine uptake among CH staff. These barriers and enablers were then mapped to the 12 domains of the Theoretical Domains Framework (TDF). Through further analysis, we categorized them into 71 barriers and 62 enablers specifically related to influenza vaccine uptake. The TDF domains most frequently mapped to were Belief about consequences (e.g., belief about the effectiveness of the influenza vaccine) (32 studies); Environmental context and resources (e.g., accessibility to vaccine (30 studies); Social influence (e.g., influence of colleagues) (25 studies); Emotion (e.g., fear of side effects) (26 studies); and Knowledge (e.g., Lack of knowledge about the vaccine the efficacy) (22 studies). No barriers or enablers were identified in the domain of "Skills" and "Beliefs about capabilities". The following sections will provide a detailed description of the TDF domains including the specific barriers and enablers within each domain that impact the influenza vaccine uptake. The domains were arranged in descending order according to the number of studies that reported factors related to each domain (Appendix B).

Environmental context and resources
Environmental context and resources were identified as barriers and enablers of the influenza vaccination. Financial resources for CH and staff are an important factor for staff influenza vaccination rate in CHs. Financial constraints [68,69,81,93] or lack of funds for vaccination [83,84] makes it difficult for CHs to provide a free onsite influenza vaccine service or improve the accessibility to the vaccine [59,60,76,88] which acts as a barrier to influenza vaccine uptake. Enablers to influenza vaccine uptake include accessibility of the influenza vaccine [64,81,91,98,73,74], availability of the influenza vaccine at a suitable and flexible time [91,96], and adequate provision of the influenza vaccine [71,96]. Countries with financial constraints encountered barriers that impacted influenza vaccination rates among CH staff, including the United States [60,61,69,71], Australia [81,83,84], and France [93]. In addition, countries facing challenges related to influenza vaccine access, such as Australia [84], Hong Kong [87], Ireland [76], Belgium [91], Italy [88], and the United States [59,65,100], also experienced difficulties in promoting influenza vaccination among CH staff. Many studies showed that a shortage of influenza vaccine supply reduced the vaccination rate among CHs [59,65,68,100]. Other studies reported that refusing the influenza vaccine due to the presence of a health condition [73,82,87,90,97,99] or allergy [66] prevented staff from getting vaccinated. A high turnover of CH staff decreases the vaccination rate among staff and prevents organizations from tracking vaccination uptake [68,71,100].

Social/professional role and identity
Sixteen studies reported barriers and enablers within this domain. Recognition that getting the vaccine was an obligation of staff's social and professional role toward residents, workplace, and others is seen as an important factor [62,71,74,75,78,84,95,[90][91][92]. CH staff who were not fully convinced and committed to their obligation to receive the influenza vaccine were less likely to get vaccinated against influenza [73,79,88,90].

Optimism
Staff were pessimistic and expressed a negative attitude towards the effectiveness [73,85,90,92] and safety [73,78,90] of the influenza vaccine, which act as potential barriers to accepting the influenza vaccine. In addition, having confidence in one's immunity can serve as a potential barrier to uptake the influenza vaccine [75,90,100].

Intention
The enabler identified as motivation to get the influenza vaccine was the presence of CH staff's intention to receive the influenza vaccine next year [62,66,73,79,91]. On the other hand, if CH staff lack the intention to receive the vaccine, it acts as a barrier and reduces the likelihood of them getting vaccinated.

Reinforcement
In the context of promoting influenza vaccination among healthcare CH staff, some of the enablers identified in the "reinforcement" domain. In four studies, positive reinforcement (e.g., social reward, incentives) was seen as a significant encouragement for vaccination [63,69,71,91]. There was strong opposition to mandatory influenza vaccination to promote vaccination uptake among care home staff [80,88].

Memory, attention and decision processes
Some CH staff cited forgetfulness as the reason for not receiving the influenza vaccine [60,88,90,92] enablers to receive the vaccine were receiving reminders [81,87,91].

Behavioral regulation
In one study, providing feedback on performance was identified as a factor that could help increase the rate of influenza vaccination among CH staff [71]. However, when there was no feedback given, it was seen as a potential barrier to improving vaccination rates [59].

Discussion
This systematic review found that although there are signs that CH staff are accepting the influenza vaccine and have positive attitudes towards it, there are also significant barriers that impede them from accessing the influenza vaccine. The results of this systematic review support the conclusions drawn from previous reviews [102], which state that the behavior surrounding vaccination is complicated and influenced by numerous factors. Our findings regarding individuals' views on vaccination align with previous systematic reviews from other health care settings, including concerns about side effects, beliefs in efficacy, and safety [42][43][44]49,50,52].
Using a comprehensive theoretical framework for understanding the behaviours of CH staff toward the influenza vaccine is helpful in providing a structured method for recognizing barriers and enablers and designing interventions aimed at improving influenza vaccine uptake [56,103].
After conducting this synthesis using the TDF, specific barriers and enablers were categorized that could be useful in targeting areas for potential interventions in the future. In addition, this review lays the groundwork for developing a customized and complex intervention to improve influenza vaccine uptake among CH staff by connecting the barriers that can be changed to the appropriate behavior change techniques (BCTs).
The majority of the studies included in this review have reported the presence of misconceptions regarding the vaccine, including concerns about its safety or effectiveness. These findings agree with other similar reviews conducted in various healthcare settings [42,50]. Interestingly, healthcare workers who were hesitant to receive the influenza vaccine expressed similar concerns as those observed during the COVID-19 pandemic, such as worries about the safety, efficacy, and potential side effects of the vaccine [104]. This suggests that educational interventions should be prioritized and should include a range of informative materials, such as leaflets, posters, and videos. These resources can effectively address potential concerns and contribute to a comprehensive understanding of influenza vaccination among care home staff [105,106]. Furthermore, encouraging open and honest communication between staff and management about their concerns and experiences with the vaccine was seen as an enabler to accept the vaccine [107].
It was observed that there is a relationship between the desire to Table 3 Quality assessment of quantitative studies (CASP): Study  1  2  3  4  5  6  7  8  9 Nace (2007)  protect themselves, their family and the patients they are caring for and acceptance of the influenza vaccine and the willingness to receive the influenza vaccine. These findings are consistent with the outcomes of previous systematic reviews conducted on the topic [43]. Therefore, incorporating information on the protective benefits of vaccines for CH staff, their relatives, and patients into educational interventions may serve as an important component of any vaccination advocacy initiative. Additionally, it is important to highlight both the potential benefits and limitations of influenza vaccines within these interventions. Acknowledging the current evidence on vaccine effectiveness, including its variations and uncertainties, can contribute to a more transparent and informed communication strategy. This approach can effectively contribute to enhancing awareness and promoting positive vaccination behaviors within the CH settings [52,108]. This review also found that having a reliable person who could provide accurate information about vaccinations was an enabler to accept the influenza vaccine. It has been found that healthcare providers may not have the time to search for information from national public health institutes [109], and this highlights the importance of providing information about the influenza vaccine, using engaging media to disseminate the information, and having a trustworthy point of contact to convey the information to the healthcare workers [105,106,110].
The low uptake of the influenza vaccine among CH staff can also be attributed to several environmental and organizational factors such as financial constraints, vaccine shortage, whereas providing financial support for CHs to make the vaccine accessible and available to staff were reported to improve influenza vaccination rate [30]. A significant barrier to influenza vaccination uptake among healthcare workers in hospital settings is the lack of accessible and convenient vaccination services [42,111]. However, research has indicated that healthcare personnel who work in CHs face greater barriers in accessing influenza vaccination compared to those who work in other healthcare settings [27].
There is a need for health systems to be more involved in supporting this sector by offering incentives or reimbursements to ensure that CHs and vaccine providers have the resources they need to provide the vaccine [112]. In addition, ensure a stable and consistent supply of the vaccine, which can be done through better planning and coordination with vaccine providers and distributors may therefore be beneficial in improving influenza vaccine rate [113].
The adverse reaction to the influenza vaccine or allergy to eggs could prevent CH staff from getting the vaccine were presented in the Environmental context and resources domain because this requires restructuring the physical environment, e.g., by offering alternative vaccines or medical interventions for staff who are experiencing this.
One of the most important motivators to get the vaccine is a supportive environment for the CH staff to get vaccinated and improving the accessibility and availability of the vaccine, especially through providing a free onsite vaccine service in a flexible schedule [59,114,115]. Also, provide support and resources to CHs to track and monitor the vaccination rate of their staff, even with high turnover rates. This can include using electronic health records or other tracking systems to monitor vaccine uptake and ensure that all staff are receiving the vaccine.
The act of getting vaccinated is a behaviour that is a complex and requires consideration of various factors, including attitudes, beliefs, motivation, perceived risk, and social and organizational influences [116]. Therefore, it is essential to understand the complex nature of vaccination and its determinants in order to develop effective strategies to encourage vaccination uptake.
Interventions aimed at increasing access to influenza vaccine, raising awareness about the vaccine, and providing incentives were found to have limited effectiveness when implemented individually [117]. Combined interventions are required as many studies indicated that a greater uptake of vaccinations among healthcare workers was achieved through the implementation of multiple interventions across various domains [48,108,118,119].
CHs can differ in terms of their context, residents, staff characteristics, services provided, and size. Furthermore, CHs can vary significantly between countries, and even within the same country, due to distinctive regulations at the national or regional level, as well as the unique needs of each geographical area [118]. Therefore, when developing interventions, theory can be used to understand factors influencing behaviour change and to determine appropriate techniques. Evidence helps decide which behaviours to target, effective behaviour change techniques, and modes of delivery. Practical considerations, such as resource availability and acceptability in the targeted setting, must also be considered [56].

Strengths and limitations
This systematic review has several strengths. Firstly, including qualitative and quantitative research provides a comprehensive understanding of the complex nature of vaccine uptake behaviour among CH staff, and highlights the valuable insights that can be gained from both approaches. Secondly, the TDF was used to gain a thorough comprehension of the factors that prevent or facilitate the uptake of the influenza vaccine among CH staff. The TDF's inclusion in the study provides a strong foundation for developing an intervention that is both evidence and theory-based.
Our study solely included studies conducted in English and predominantly consisted of research carried out in North America and European countries. As a consequence, there is a potential restriction on the general applicability of our findings to alternative settings, particularly with regard to organizational culture. In our study, we included factors from surveys that were considered relevant even if they were indicated by less than 10 % of the participants. We made this decision because our aim was to provide a comprehensive overview of the barriers and enablers to the influenza vaccine uptake among CH staff. By considering all factors, even those endorsed by a small proportion of participants, we sought to ensure that we captured a broad range of perspectives and potential influences on the phenomenon under investigation. Many studies included in this systematic review relied on surveys to explore barriers and enablers to influenza vaccine uptake among CH staff. While this methodology allows for standardized data collection, it also introduces the possibility of bias as the pre-determined questions may reflect the authors' beliefs.

Recommendations for future research
The findings of this review emphasize the importance of developing interventions that target multiple levels, including individual and organizational factors. One potential approach is to use the TDF domains identified in this review to develop a taxonomy of behaviour change techniques (BCTs) that are likely to be effective in promoting influenza vaccination uptake among CH staff. This taxonomy could then be used in collaboration with stakeholders to identify the most appropriate BCTs and tailor interventions to the specific needs and context of CHs. APEASE (Affordability, Practicability, Effectiveness and costeffectiveness, Acceptability, Side effects/safety, Equity) could be used as a framework for assessing the feasibility and appropriateness of these interventions, ensuring that they are effective, practical, and acceptable to the CH staff and other relevant stakeholders [120]. Finally, the interventions could be tested in feasibility and definitive trials to evaluate their effectiveness and potential for implementation on a larger scale.

Conclusion
This systematic review provides a comprehensive overview of the barriers and enablers affecting the uptake of influenza vaccine among CH staff. Multiple theoretical domains are likely to play a significant role in influencing vaccination uptake among CHs staff. Several barriers and enablers were identified at the individual, organizational levels. The findings of this review emphasize the importance of understanding the complex nature of vaccination behaviour and developing strategies that combine various interventions across different domains.

Funding
This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

Declaration of Competing Interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

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Theoretical domain framework

Professional roles toward residents
Lack of awareness of professional role [90] toward residents [88] Awareness of professional role toward residents [62,75,78,84,95,91,92] responsibility of staff to get vaccinated Lack of belief in the role and responsibility of HCW to get vaccinated [73,79,88,90] • Belief in the need/responsibility of staff to get vaccinated [91,96] every year [74] • Belief that vaccination is their duty [79] Social role and responsibility Lack of awareness/lack of social role to protect others [88,90] Awareness of social role to protect others [62,75,78,89,90] Organizational commitment Awareness of professional role toward workplace [71,74,91,92] Cultural identity Lack of believe in immunization [68]

Optimism (12 studies)
Optimism about the efficacy of influenza vaccine Lack of confidence in the efficacy of influenza vaccine [73,85,90,92] Confidence in the efficacy of the influenza vaccine [89][90][91] Value of the influenza vaccines Pessimism about the value/usefulness of vaccines [91] Optimism about the value of influenza vaccine [78] Trust vaccine • Lack of trust in vaccine safety [73,78,90] • General lack of trust in influenza vaccine [68,72] scepticism [83] Trust vaccine safety [89] Identity Confidence in own immunity [