Vaccine promotion strategies in community pharmacy addressing vulnerable populations: a scoping review

Abstract

Context

Social determinants of health are drivers of vaccine inequity and lead to higher risks of complications from infectious diseases in under vaccinated communities. In many countries, pharmacists have gained the rights to prescribe and administer vaccines, which contributes to improving vaccination rates. However, little is known on how they define and target vulnerable communities.

Objective

The purpose of this study is to describe how vulnerable communities are targeted in community pharmacies.

Methods

We performed a systematic search of the Embase and MEDLINE database in August 2021 inspired by the Preferred Reporting Items for Systematic Reviews and Meta-Analyses protocols (PRISMA ScR). Articles in English, French or Spanish addressing any vaccine in a community pharmacy context and that target a population defined as vulnerable were screened for inclusion.

Results

A total of 1039 articles were identified through the initial search, and 63 articles met the inclusion criteria. Most of the literature originated from North America (n = 54, 86%) and addressed influenza (n = 29, 46%), pneumococcal (n = 14, 22%), herpes zoster (n = 14, 22%) or human papilloma virus vaccination (n = 14, 22%). Lifecycle vulnerabilities (n = 48, 76%) such as age and pregnancy were most often used to target vulnerable patients followed by clinical factors (n = 18, 29%), socio-economical determinants (n = 16, 25%) and geographical vulnerabilities (n = 7, 11%). The most frequently listed strategy was providing a strong recommendation for vaccination, promotional posters in pharmacy, distributing leaflet/bag stuffers and providing staff training. A total of 24 barriers and 25 facilitators were identified. The main barriers associated to each vulnerable category were associated to effective promotional strategies to overcome them.

Conclusion

Pharmacists prioritize lifecycle and clinical vulnerability at the expense of narrowing down the definition of vulnerability. Some vulnerable groups are also under targeted in pharmacies. A wide variety of promotional strategies are available to pharmacies to overcome the specific barriers experienced by various groups.

Introduction

The COVID-19 pandemic has shed light on vaccination discrepancy between and within countries as we had both the technical and financial means to vaccinate individuals of every country [1]. It is estimated that 234,00 deaths could have been prevented in the US between June 2021 and March 2022 with a primary series of vaccinations [2]. Low vaccination rates disproportionately affect communities commonly defined as “vulnerable”. According to the Center for Disease Control and Prevention, infants from families with income below the poverty line are 30% less likely to receive the 7 recommended vaccines (measle-mumps-rubella, diphtheria-pertussis-tetanus, polio) for children aged 19–35 months [3]. Revenue is not the only factor influencing access to vaccination. Vaccination underservice directly affects communities’ health; as Black, Indigenous and Hispanic individuals in comparison with non-Hispanic White individuals have higher influenza-related hospitalization rates [4]. Population health is directly linked to the upstream societal structures and institutions that shape communities, to the relationship between individuals and to health seeking behaviours [5]. Vulnerability to infectious diseases can be associated to individual characteristics (e.g. age, pregnancy, disease state, disability), to habits (e.g. sexual practices, use of alcohol, illicit drug use, travelling) or to wider determinants such as social status, physical environment or social support [6].

In recent years, vaccination in community pharmacies is gaining momentum and may present a solution to reduce vaccine disparity. Pharmacists are recognized as accessible, convenient, trustworthy and cost-effective vaccine providers [7,8,9,10]. Studies from various jurisdictions show that allowing pharmacists to vaccinate increases uptake [11,12,13,14]. Pharmacies have surpassed medical offices in the provision of flu vaccines in the United States and in Canada [15, 16]. Prior reviews have focused on vaccine acceptability, accessibility and vaccine uptake following policy to allow pharmacists as immunizers [10, 17,18,19,20]. To our knowledge, no review has been conducted on how pharmacists reach eligible communities. Pharmacies are privately owned businesses and although pharmacists are dedicated to the well-being of their patients, some commercial practices may not be aligned with public health objectives of reaching those who need it the most. Certain pharmacies seem to adopt proactive methods to target vulnerable communities while others may rely on a ‘’first come first serve basis’’ [21]. As key contributors to vaccination, pharmacists must revise their implicit and explicit assumptions since it impacts how they define and reach vulnerable populations through their vaccine services [22]. Indeed, public health research has shown that “vulnerable populations” are not fixed identities, but the result of a process, which should be questioned from the perspective of vaccine services delivery in community pharmacies.

Evidence on the characteristics of patients vaccinated in pharmacy settings suggests that pharmacies vaccinate a more privileged population during influenza mass campaigns. Pharmacies tend to vaccinate individuals with a higher income [23, 24], higher education [24, 25] and younger populations [14]. Other traits such as being immigrant [23, 26], having diabetes or hypertension [23] and having a high number of chronic diseases [25] meant individuals were more likely to obtain their vaccine in a physician’s office. As definitions of vulnerable populations are multiple and go beyond clinical condition factors, understanding what characteristics pharmacists perceive as vulnerable remains key. The perception of vulnerability trickles down into how pharmacies target vulnerable populations, when they do, and may help finding solutions to vaccine discrepancy.

Objective

Our objective is therefore to describe how vulnerability is defined and how vulnerable communities are targeted in community pharmacies within the published literature. More precisely, we seek to meet the following 4 objectives:

• 1) Describe the studies on the vaccination of vulnerable communities in pharmacies;

• 2) Identify which vulnerability characteristics are used to target underserved communities;

• 3) Document the barriers and facilitators towards vaccinating vulnerable communities in pharmacies;

• 4) Discuss which strategies are used by pharmacists and their team to target vulnerable communities.

Methods

Based on the framework of scoping studies, our work seeks to describe, identify and synthesize the gaps in the existing literature [27]. Scoping reviews are useful to map out the existing literature on newer topics and orient future research. In our case, this review will allow us to better understand how pharmacists conceive vulnerability and how it impacts their implicit or explicit actions to address vaccine discrepancies. This scoping review will also determine the value of undertaking a full systematic review. We followed the checklist from the Preferred Reporting Items for Systematic reviews and Meta-Analyses extension for Scoping Reviews (PRISMA- ScR) [27]. With the help of an experienced librarian, we identified the relevant keywords and MeSH on the following 3 topics: ‘vaccination’, ‘pharmacy’ and ‘vulnerable populations’. The search strategy was then elaborated for the Embase database and adapted according to the MEDLINE database.

Search strategy

The search was performed on 16 August 2021 to identify all articles in English, French or Spanish addressing vaccination of vulnerable communities in a pharmacy setting. We chose not to limit our study to a specific time period. This allowed gathering data from countries or states at different legislative stages regarding the status of pharmacists as prescribers and vaccinators. Inclusion criteria for this scoping review are the following: a) articles in a community pharmacy setting; b) articles where vaccination targets a population defined as vulnerable to an illness targeted by the vaccine; and c) peer-reviewed quantitative or qualitative studies or reviews studies.

Exclusion criteria are: a) articles providing insufficient details on vaccination in a pharmacy setting; b) vaccination by a pharmacist that occurs outside of a community pharmacy setting; c) articles where vaccination was not the primary focus; d) vaccine guidelines for healthcare professionals.

Data extraction

Articles were imported into Zotero for duplicate removal, initial screening of titles and abstracts. The main author and one coauthor independently screened the initial 100 articles to reach a kappa consensus coefficient above 80%. Discrepancies were resolved through consensus. The remaining articles were sorted by the main author and uncertain articles were debated with a co-author. For feasibility purposes, data were extracted by one member with the use of a grid validated by co-authors.

The data extracted are comprised of the publication year, the methodology, the study population, the target strategy, the outcomes, and the barriers and facilitators reported by the authors. Results were then compiled, and descriptive statistics were generated through Excel software. The various target strategies were classified according to emerging categorization of passive, active and indirect promotion tactics. We finally identified the specific barriers to each vulnerable group and matched them with promotional strategies that overcome them. A quality of appraisal was not undertaken due to the anticipated heterogeneity of studies.

Results

Article overview

After performing the initial search, 1,039 articles were identified (Fig. 1). We found 614 articles originating from the Embase database and 425 from the MEDLINE database. We removed 227 articles due to duplication within or across databases. The 812 remaining articles titles were screened, and 444 articles were removed because vaccination was not a central topic in the research. The remaining 368 articles were screened through their abstract and 295 articles were discarded because they did not address a population considered as vulnerable. The remaining 73 articles were fully read, and 10 articles were discarded since they occurred outside of a pharmacy setting, were not original research or focused insufficiently on vaccination or on a vulnerable population. The 63 included studies are presented in Table 1.

Fig. 1

Study Selection Process Flowchart

Table 1 Summary of Peer Review Articles Included in the Scoping Review

Most of the articles obtained were current, as 44 articles were published after 2014 (69.8%) (Table 2). Studies become scarcer as the further we investigated back in time. Eleven articles date from 2010–2014 (18%), 3 articles from 2005–2009 (5%) and 5 articles were published before 2004 (8%). No article included in our scoping review was published before 2000. Most articles originated from North America (n = 53, 84%) and a few articles came from Europe (n = 6, 10%) and Oceania (n = 2, 3%). Articles from North America collected data almost exclusively in the United States (n = 50, 79%). Three articles were conducted in Canada (5%). In Europe, articles originating from the United Kingdom (n = 3, 5%), Belgium (n = 2, 3%) and Spain (n = 1, 2%) were reported. One article was published from Australia (2%) and one from New Zealand (2%).

Table 2 Included study characteristics

The studies showed a wide variety of study designs with a predominance for quantitative frameworks (n = 48, 76%). A smaller portion of studies used qualitative design (n = 4, 6%), mixed-methods design (n = 6, 10%) and literature reviews methodologies (n = 5, 8%). When looking more into the methodology of quantitative studies, cross-sectional surveys were the most common (n = 16, 25%), followed by quasi-experimental studies pre-post design (n = 9, 14%), implementation studies (n = 7, 11%), cohort studies (n = 6, 10%) and randomized control trials (n = 5, 8%). Other quantitative designs such as comparison quasi experimental studies, case–control studies and geospatial analysis were less frequent (n ≤ 3). Qualitative studies all used semi-structured interviews to collect their data. Most of the mixed-methods studies were implementation studies (n = 4, 6%). Out of the 5 review articles (8%), 2 were systematic reviews (3%) and 3 were narrative reviews (5%). The objectives and outcomes of various studies differed greatly. Almost a third of the studies evaluated the vaccination uptake generated by different interventions in community pharmacies (n = 20, 32%).

The influenza vaccine was reported in almost half of the studies (n = 29, 46%). Herpes zoster, pneumococcal and human papilloma virus vaccines were each discussed in 14 studies (n = 22%), followed by tetanus-pertussis-diphtheria (n = 6, 10%) and travel vaccines (n = 2, 3%). Other vaccines figured in lower frequencies such as meningococcal vaccines, hepatitis A and B, measles-mumps-rubella or other children’s vaccinations (n ≤ 2). Thirteen studies investigated more than one vaccine at a time (21%). All but one combined the influenza vaccine with one or many other vaccines (n = 12, 19%). The combinations were influenza-pneumococcal (n = 4, 6%), influenza-pneumococcal-herpes zoster (n = 2, 3%), influenza-pertussis (n = 1, 2%) or a combination of more than 3 vaccines (n = 6, 10%).

Vulnerability categories

We divided the various vulnerable populations into 5 categories of vulnerability: lifecycle vulnerabilities (n = 48, 76%), clinical factors (n = 18, 29%), socio-economical determinants (n = 16, 25%), geographical vulnerabilities (n = 7, 11%) and others (n = 6, 10%) (Table 3). A total of 22 articles combined more than one vulnerability category (35%).

Table 3 Frequency of vulnerability characteristics

First, within the lifecycle category, age-related criteria were the most prevalent such as being elderly (n = 25, 40%), adolescent (n = 12, 19%), of childbearing age (n = 3, 5%) or being a child (n = 2, 3%). Other subcategories within the lifecycle category include vulnerabilities around pregnancy and parenthood such as pregnant women (n = 4, 6%) and parents of children (n = 2, 3%).

Second, the clinical factors category regrouped a wide range of illnesses that increase the risk for complications such as pulmonary conditions (n = 4, 6%), diabetes (n = 3, 5%), cancer (n = 1, 2%), cardiovascular disease (n = 1, 2%) or a combination of at-risk illnesses or an immunocompromised status (n= 9, 14%). Illness status was identified via medical databases, insurance databases, pharmacy databases and self-reported medical history. One study defined its vulnerable population solely by the pharmacological profile by including patients that take more than 3 chronic medications [48]. One study also studied vaccination outcomes within a chronic condition management program [36].

Third, in the socio-economic determinants category, vulnerability is targeted through race (n = 8, 13%), income (n = 6, 10%) and education (n = 3, 5%). In most race-based studies, race was used to differentiate the proportion of users that obtain their vaccination in a pharmacy versus a medical setting. Some articles segmenting the study population with income focused on insurance status such as underserved adults (n = 2, 3%) [73, 83] or Medicaid beneficiaries (n = 2, 3%) [28, 35].

Fourth, geographical vulnerabilities were most often defined by contrasting rural and urban residence localization (n = 4, 6%). Other studies used a more precise categorization linked to accessibility such as medically underserved areas (n = 2, 3%) or social determinants of health such as low socio-economic status area (n = 1, 2%), racially and ethnically segregated neighborhoods (n = 1, 2%). One study (2%) used the state of origin [26] to contrast states where pharmacists are able and unable to administer vaccines.

Finally, the last category includes other vulnerabilities that did not fit in the previous categories such as occupation (n = 3, 5%), lifestyle (n = 2, 3%) and individuals with incomplete vaccination status (n = 2, 3%). Groups included in the occupation subcategory were military personnel, healthcare workers and students. The studies in the lifestyle category discussed travellers going to high-risk destinations. It is important to note that a third of the articles (n = 23, 37%) combined two or more vulnerability categories. The most common combination was clinical factors and lifecycle vulnerabilities (n = 14, 22%).

Vaccination barriers and facilitators

Twenty-four barriers and 26 facilitators were compiled from the included articles (Table 4) and classified according to 5 levels (Fig. 2): 1) patient level (individual characteristics and perceptions), 2) interpersonal level (relationship between patients and pharmacy team members), 3) organizational level (factors within the pharmacy organization), 4) health system level (interaction between healthcare organizations, distributors and coverage providers) and 5) policy level (legal and political context) (Fig. 2).

Table 4 Frequency of barriers and facilitators

Fig. 2

Vaccination Barriers and Facilitators in Community Pharmacy

Barriers were proportionally distributed amongst levels. Fifteen articles (24%) identified barriers originating from the patient’s lack of knowledge on vaccines or eligibility unawareness. Third-party reimbursement and the lack of coverage were also listed as a barrier in 13 articles (21%). Organizational obstacles such as other competing priorities (n = 15, 24%), missed opportunities (n = 11, 18%) and the requirement of a prescription from a physician (n = 9, 14%) were also mentioned.

Interestingly, interpersonal level facilitators were reported almost twice as often as other categories. Providing a strong recommendation for vaccination to a vulnerable patient was the most common facilitator and stated in 28 articles (44%). Other organizational helpers were utilizing a cost-saving or a promotional method that is tied to financial incentives (n = 14, 22%) or providing convenient modalities (walk-in, extended hours) to patients (n = 12, 19%). Many articles also stated health system facilitators such as collaboration with other providers (n = 13, 21%), collaboration with public health (n = 11, 17%) and the physical accessibility of pharmacies (n = 11, 17%).

Targeting methods

Almost all of the included studies addressed interventions led by pharmacists (n = 60, 95%). The remaining 3 articles only involved pharmacy students (n = 2, 3%) and technicians (n= 1, 2%). Two studies described a clinical education program that was managed by pharmacy students, but under the supervision of pharmacists (3%) [33, 69]. One study reviewed the role of pharmacy technicians in gaping vaccination discrepancies [64]. Pharmacy technicians can contribute in bridging the discussion between pharmacy services and vaccination, keeping track of vaccination refusal and assisting in administrative tasks (documenting vaccines in the immunization records, collecting patient history, preparing the billing…). Eight articles (13%) also underlined the key role of pharmacy technicians in initiating the conversation about vaccination with eligible patients or referring to the pharmacist for further questions [29, 36, 42, 44, 64, 66, 69, 85].

Targeting methods can be defined as the tactics employed to identify, reach and distribute a service or a product to a specific group [86]. Twenty-three targeting methods were identified and divided between 3 categories: active promotion (14 strategies), passive promotion (6 strategies) and indirect promotion (3 strategies) (Table 5). Active promotional methods were diverse and involved the pharmacy team actively engaging and interacting with selected patients to promote vaccination [87]. The most common active promotion strategy was providing a strong recommendation for vaccination to patients (n = 25, 40%). Other strategies were distributing a bag stuffer or pamphlet (n = 17, 27%), initiation of a conversation on vaccine by a pharmacy team member (n = 8, 13%), sending a personalized letter (n = 8, 13%) or giving a personalized phone call to a vulnerable patient to promote a vaccine (n = 5, 8%). Some strategies were designed within the pharmacy workflow such as screening patients as they picked up the medication (n = 7, 11%) or programming a nudge in the pharmacy software notifying the pharmacists of an eligible patient (n = 4, 6%). Other strategies were better suited outside of the pharmacy workflow such as generating a list of eligible patients to offer them a vaccination appointment (n = 9, 14%), screening during another program such as a medication therapy review, a COPD medication review program or when receiving another vaccine (n = 6, 9.5%) or sending them an automated promotional phone call (n = 1, 2%). Some strategies aimed to educate patients through the distribution of an informational leaflet (n = 17, 27%) or providing educational group sessions to vulnerable patients (n = 3, 5%). Many articles reported collaboration with physicians (n= 13, 21%) such as recommending a vaccine to the patient’s physician, proactively asking them for a prescription or providing vaccination through a collective order. A collective order allows a health care professional that cannot prescribe vaccines to obtain a prescription signed by the responding physician without being evaluated by this physician [88]. One article addressed financial barriers by providing free influenza vaccine vouchers to underprivileged adults through community organisations (2%).

Table 5 Frequency of targeting strategies

Passive promotion strategies reach patients through smart positioning, media presence or a third party that does not directly generate an interaction with the pharmacy [87]. Within this category, we found the use of classic promotional methods such as a poster in pharmacies describing vaccination services, newspaper, TV and radio advertising (n = 6, 9.5%). Some articles reported promotional strategies using social media marketing (n = 3, 5%). Promotion was also done through word-of-mouth by patients and staff (n = 2, 3%) as well as through neighborhood health professionals (n = 4, 6%). Pharmacies also provide convenient modalities for vaccination such as walk-in and extended hours especially during mass influenza campaigns (n = 4, 6%).

Finally, some strategies were identified as indirect since they targeted the pharmacy staff instead of the patients or the vaccination process. Staff training (n = 8, 13%) was listed as an efficient method to make the pharmacy staff vaccine ambassadors. Teachings included improving knowledge on vaccines, providing assertive communication training and vaccine process training. Ensuring a culturally relevant communication (n = 3, 5%) was a way to improve how the message is perceived by the population. Finally, one article mentioned the use of customized prescription pads (2%) to facilitate the integration of vaccination within the pharmacy workflow.

Drawing from the previous data, we synthesized the barriers and promotional strategies to help pharmacists overcome vaccination challenges. We associated each vulnerable population to the common barriers identified in the included articles (Fig. 3). Those barriers were then linked to vaccination promotion strategies. We will first look at barriers and strategies that concern specific vulnerable populations. Pharmacists presented knowledge gaps with vaccines addressed to children and individuals with chronic conditions [48, 89]. These can be addressed through training on these specific populations [75]. Vaccine hesitancy, negative attitudes and personal beliefs against vaccines require time and an understanding the patient’s viewpoint [33]. A conversation between the pharmacist and the patient gives an opportunity to correct misconceptions, provide a strong reference for vaccination and call for action [34]. Timing issues such as not reaching pregnant women during their 3^rd trimester to offer pertussis vaccination [42] can be addressed by carefully monitoring the pharmacy’s population for vaccine eligibility through list generation or screening candidates during the workflow [44]. For patients that lack time to discuss or obtain a vaccine, pharmacists may rely on advertising and interprofessional collaboration to encourage patients to contact the pharmacy at a more convenient time for them [23]. Barriers to social-demographic determinants such as lack of coverage may be dealt with through facilitating reimbursement procedures with insurance [67] or through offering vouchers [45]. Trust may also be reinforced through relationship building with the pharmacy team and culturally relevant communication [28, 42, 64]. Providing convenient modalities for vaccination through walk-in or extended opening hours may reduce accessibility constraints that are frequent in rural areas [53, 73].

Fig. 3

Promotion Strategies to Overcome Specific Barriers of Key Vulnerable Groups

We identified 4 barriers that were common to every vulnerable category. The lack of a strong provider reference can be addressed by better linking patients to pharmacists through conversation initiation by the pharmacy team. Pharmacists and their team may overcome the lack of awareness to vaccines from vulnerable populations by actively screening patients in the workflow [44, 51], soliciting other health professional [50] or creating a list of eligible patients and contacting them through a letter or a phone call [36, 39]. To reduce missed opportunity, vaccination promotion should be discussed as a pharmacy team and involve every employee [42, 64, 66, 85]. A reminder system should be planned to reduce missed appointments and opportunities through notes in the file or nudges [37, 89]. An effective way to address competing priorities within the busy workflow is to move the workload outside of the regular distribution activities [30]. Designating a champion or key tasks to specific employees such as listing the eligible patients can help keep focus on vaccination through pharmacy activities [71].

Discussion

This scoping review identifies a wide variety of studies targeting different populations considered as vulnerable by community pharmacists. Vaccinating vulnerable communities is dominantly studied in the United States where health discrepancy between race, economic status and geographical location are wide [4]. American pharmacists also benefit from decades of expanded scope of practice [90] which correlates with the wide body of articles published after 2014 (n = 44, 69.8%). We suspect that other regions of the world were underrepresented due to the language inclusion criteria and since pharmacists are predominantly involved in medication dispensing activities rather than clinical activities such as vaccination.

Vaccination has been a traditional activity of public health instances and pharmacists feel pressured to justify their value as efficient immunizers [10]. This has been observed in our review as more than a third of the studies have evaluated the vaccination uptake of pharmacists’ led interventions (n = 20, 31%). Qualitative and mixed-method studies provided a rich understanding of the dynamic of vaccination within the dispensing-centered mindset of pharmacies.

The challenges of defining vulnerable communities

Pharmacists and their team target vulnerable communities in the included studies mainly based on life cycle criteria and clinical factors. They rely on the information that is available to them to assess eligibility. Age remains the most convenient method to target individuals but may oversimplify the rationale on risk prevention. On one hand, age provides a good statistical predictor of developing an illness such as influenza or pneumonia complication [91, 92]. Therefore, it appears fair to allocate more resources to better protect elderly populations. On the other hand, age may be a flawed indicator as life expectancy varies according to geographical localization or socio-economic determinants. Indeed, the gap in life expectancy varies according to income [93], education [94] and race [95] in the US. Disparities in life expectancy between rural and urban areas is however growing in the last 20 years and is attributable to cardiovascular and drug-overdose death [96]. Deciding on a cut-off to recommend a vaccine becomes a difficult exercise as years saved vary greatly according to the circumstances of each individual. Moreover, geriatric medicine is moving towards frailty score rather than age as means to aid in clinical decisions [97]. Many frailty scales provide a more detailed understanding of life expectancy or risk of complications, but have not been used in the field of vaccination.

Elderly people are also affected by the immunosenescence phenomenon which can be described as the waning of innate and cellular immunity [98]. The capacity to generate immunity is also affected by the clinical profile of a person. Some chronic diseases such as depression, cardiovascular diseases or conditions such as malnutrition, femur fracture or stress may decrease our capacity to generate immunity for a certain period of time [98,99,100]. Vaccinating while younger or prior to developing stress inducing conditions may be advantageous. Although scientific evidence on vaccination is complex, generating vaccination guidelines must remain simple for clinicians and easy to communicate to the public.

The list of chronic conditions affecting patients is not always easy to obtain in the community setting as diagnoses are seldom shared with the pharmacist. Pharmacists document in the patient’s pharmacological profile according to patients’ self-reported illnesses or by inference based on the patient’s medication. This process remains imperfect. One study directly used the number of medications as a mean to identify at-risk patients [79]. Correlating the number of medications provides a flawed view of vulnerability as some conditions such as single pathology like diabetes may require a combination of four or more oral treatments, while several other conditions may be targeted by a single tablet that contains a combination of drugs (e.g. antihypertensive and cholesterol lowering). Technological advancements and better diagnosis sharing between health professionals are ways to spend less on assessing a patient’s eligibility and more on promoting vaccination. As examples, suggestions range from a universal vaccine registry, to sharing the accesses to the pharmacological and medical file, to simplifying the eligibility criteria [50, 53, 63].

Other vulnerable groups provide their own targeting challenges. Considering that nearly half of all pregnancies in the US are unplanned [101], efforts to ensure adequate vaccination during pregnancy should be extended to all women of childbearing age. Prevention is however a wide concept, and the definition of at-risk groups widens as we discover additional risk factors. More and more, asymptomatic individuals with risk factors are treated with pharmacological drugs such as in hypertension or dyslipidemia which modifies our conception of health and sickness. Vaccines are also preventive medicines. In many jurisdictions, pharmacists are not able to actively participate in the preventions recommended in pregnancy as they cannot prescribe or administer vaccines against pertussis or other conditions within the regular vaccination calendar. Similarly, adolescents are the subject of many studies in our scoping review and the challenges rely on communication difficulty and patient unawareness of vaccination needs [33, 68]. Having a dual audience, both adolescents and their parents, confronts stereotypes and perceptions on sexuality which pharmacists and their team may feel uncomfortable to address. The timing to receive the vaccine does not always correlate with the optimal time to influence parental decision. More opportunities to discuss vaccination earlier on during childhood and schooling are necessary to increase vaccination uptake in adolescent and pregnant populations.

Social determinants of health and geographical factors are less frequently used to target vulnerable populations according to our results. From a pharmacy perspective, data on education levels and income are not readily available during workflow operations, which makes targeting for these vulnerabilities difficult. Conducting studies on adherents of an insurance program such as Medicaid [28, 35] appears to be the simplest way to study income disparities. Few studies attempt to target other individuals in precarious financial situations such as uninsured adults that do not qualify for Medicaid or underinsured students. Limited solutions are identified to overcome uninsured individuals. Addressing cost is one way to encourage vaccination by providing free vouchers to uninsured patients [45]. The cost of the program were assumed entirely by the pharmacy chain as part of a corporate social responsibility strategy, providing benefits to public health and promoting pharmacies as healthcare establishments [45]. Patient targeting was done with the help of community organizations and required readjustments on the 2nd year as redemption of the voucher was low (52% in 2015/2016 vs 87% in 2016/2017) [45]. Alternatively, many studies focus on access barriers to vaccination as less wealthy clienteles often require more flexible times and convenient modalities to access services. Vulnerability characteristics beyond age and chronic condition are therefore seldom integrated into targeting practices which shows a narrow understanding of vaccine disparity determinants.

The forgotten groups

It is worth mentioning the absence of other marginalized communities from the scoping review, such as gender, sexual orientation and other marginalized communities. Females were targeted in studies that discussed vaccines specific to pregnancy or adolescence, which aligns with specific vaccine indications. However, no studies designed interventions to minimize vaccination discrepancy between men and women. Indeed, females are 42% more likely to receive an influenza vaccine then males when adjusted for common confounding factors [102]. Vaccine response also varies according to gender. When vaccinated against influenza, elderly women displayed greater humoral response against common flu lineage than elderly men, supposing a greater protection [103]. We must therefore understand that vulnerability goes beyond the mere expression of biological characteristics; we can seek answers in the structural construction of inequalities between groups.

Although specific LGBTQ key words were included in our search, no studies targeting this marginalized community came out. Men who have sex with men are disproportionately at risk of sexual transmitted disease which makes them candidates for Hepatitis B and HPV vaccines [104, 105]. Vaccines such as HPV address a sensitive topic, and pharmacists express discomfort discussing sexual health matters in a pharmacy setting [68]. Even though pharmacists are accessible health professionals, LGBTQ communities are reluctant to divulge their orientation due to fear of judgment or lack of confidentiality [106]. More efforts are needed to make pharmacies an inclusive and safe environment. Positive actions towards inclusivity can be displayed through offering information pamphlets specific to LGBTQ stakes, communicating with inclusive vocabulary or showing support to the community [107].

Other hard-to-reach communities such as injectable drug users, patients receiving an opioid agonist therapy or homeless people are at higher risk of infection and thus good candidates for vaccination [108]. These populations are often stigmatised by many societal institutions and are less inclined to be offered and receive preventative services. Community pharmacies may have better opportunities than other health care entities to build a trusting relation with these individuals due to easy access. Some opportunities may present themselves during dispensing activities for example when distributing clean needles, naloxone kits or other medications.

Facilitating vaccine promotion

Barriers identified regarding vulnerable groups were consistent within the literature in other contexts than in pharmacy. In the context of pregnancy, two such examples are the fear of adverse pregnancy outcome and the failure to recommend vaccination [109]. The knowledge gap from healthcare providers is listed as an important barrier [110, 111]. Patients unaware that a vaccine is recommended often wanted to contact their family physician before obtaining the vaccine, which delays vaccination. This reason was cited as a common barrier in the studies we reviewed and increased the risk of not pursuing the vaccination [44]. Although pharmacists are trustworthy professionals, they may be competing with the existing relationship that patients build with other health professionals [69]. The requirement for a prescription in many jurisdictions also contributed as a supplemental barrier that made vaccination less convenient in a pharmacy than at the physician’s office [38, 44]. Interprofessional collaborations remain a well noted facilitator in vaccination [21] and healthcare professionals should unite their voice to carry out a cohesive message supporting vaccination.

In the past decade, community pharmacies are transitioning from a dispensing business model to increased clinical services [112]. Although role expansion is stimulating, pharmacists are trained to consider the medication profile as a primary source of information rather than contextual and social vulnerabilities. Chronic conditions become a proxy to vulnerability at large and may simplify the interrelations between illnesses and other social determinants of health that impact access to vaccination. Organizational barriers are frequently reported and center around missed opportunities and competing priorities. Pharmacists have traditionally been reactive vaccinators [21]. This can be attributed to the fact that routine assessment of vaccination status was never a responsibility attributed to pharmacists up until recently. Although active promotional strategies were more frequently cited than passive strategies in the peer-reviewed literature, we have doubts that this reflects the pharmacy practice in the real world. Proactivity in pharmacy is often expressed through the display of posters and handing out informational leaflets [42] which alone are poor methods to impact behavioral change [113]. Many pharmacies may also not establish a formal targeting plan. This may result in voluntarily or involuntarily favouring privileged clienteles. A dispensing centered mentality pushes pharmacists towards reacting to patient’s demand instead of acting proactively. Pharmacies often rely on a ‘’first come, first serve’’ prioritization strategy which accentuates vaccine discrepancies of vulnerable communities [114]. Technology should be utilized to assist vaccine operations such as booking appointments and accessing vaccination history. Pharmacies should also make their dispensing operation more efficient to free time for value-added activities such as targeting at-risk patients. Pharmacists can plan vaccination outside of the pharmacy workflow and solicit the help of pharmacy technicians to identify eligible patients and initiate the conversation on vaccines [30]. As vaccine hesitancy is a growing concern, health professionals need to invest time and energy to educate patients on vaccines safety and effectiveness [115].

Promotional efforts made by pharmacists are complementary to governmental, public health and pharmacy chains advertising. The effect of different communications according to race on attitudes towards pneumococcal vaccination was investigated [43]. Non-White adults were less likely to follow medical recommendations and more likely to desire vaccination when the message combined duty to family and friends, fatality or safety [43]. More research is therefore necessary to better understand the core values of different populations and investigate how they were made “vulnerable” to adapt how we reach these patients. Our review highlights the importance of a strong recommendation for vaccination by pharmacists and was confirmed in a recent review on vaccine acceptance [43]. Although the efficiency of many strategies lacks proof, utilizing a combination of different strategies and providing a strong recommendation from a health provider are known as the most effective ways to encourage vaccination [116]. As pharmacists build strong relationships with their clientele, they must mobilize their team to create opportunities for a tailored conversation about vaccines and utilize their position as one of the most accessible healthcare professionals.

Limitations

First, our search strategy included 2 databases and may have overlooked some articles in the literature. Other databases could have been included such as Scopus or Web of science, but they usually provide similar results. References from the included studies could have been reviewed to find additional relevant publications. Second, our review only included published articles from the literature and did not include gray literature which may also hold valuable information regarding targeting practices in pharmacy. Third, our study targeted vulnerable communities from the perspective of pharmacies. Barriers to promoting vaccination and promotional methods are therefore subject to a selection bias within the different efforts carried out by public health instances. The search was also performed before the COVID-19 mass campaigns which allowed pharmacists to take part in vaccination efforts. Barriers and facilitators may therefore be different after the COVID-19 pandemic response. Fourth, our sample agglomerated heterogenous articles in terms of methodology, main topic, and the vaccines they discussed. Some conclusions must therefore be interpreted with caution as the reality of different vulnerable groups and vaccination may vary.

Conclusion

Throughout the last two decades, pharmacists have increasingly been involved in vaccination activities. Our scoping review highlights the use lifecycle and clinical dimensions to define vulnerability and to target patients identified as vulnerable, at the expense of narrowing down the definition of vulnerability and its process. Social determinants of health such as one’s race, income and geographical situation are important contributors of vaccine inequality. Indeed, some marginalized groups are absent form the vaccine promotion literature in pharmacy such as intravenous drug users, the LGBTQ community and homeless people. Targeting such communities requires an intricate knowledge of the barriers to vaccination, that range from a lack of access, awareness of vaccination, misconceptions to financial obstacles. A variety of active, passive, and indirect targeting methods were used by pharmacists through various vaccination initiatives. We linked them to the main barriers experienced by different groups. Pharmacists are trusted health professionals and as valuable contributors to public health goals; it is their responsibilities to include vulnerability concepts into their targeting initiatives integrate.

This review should inspire researchers to further expand our knowledge on how to define vulnerable communities in vaccination to better serve them. A conversation between public health and community pharmacies representative is much needed in this respect. Although studies center around influenza vaccination, more research is needed to better understand the drivers and the facilitators to vaccination programs for other vaccine preventable diseases, including industry-based strategies. Vaccination organization varies according to pharmacies and jurisdiction and has repercussions on the clienteles targeted by pharmacists. A deeper understanding of how pharmacists interact and collaborate with different entities will also aid policy makers and public health representatives to better align incentives to desired outcomes. Improving stagnating vaccination rates requires a collaborative effort from all pharmacy employees as well as a continuous reflection exercise on the efforts made to attract underserved communities. Pharmacists can play an even greater role in vaccination through leveraging their position as accessible, competent, and trustworthy health professionals.