Practices and Perceptions of Community Pharmacists in the Management of Atopic Dermatitis: A Systematic Review and Thematic Synthesis

Understanding the contributions of community pharmacists as first-line health providers is important to the management of atopic dermatitis, though little is known about their contribution. A systematic review was carried out to examine practices and perceptions of the role of community pharmacists. A literature search was conducted in five different databases. Full-text primary research studies, which involved practices and perceptions of the role of community pharmacists in the management of atopic dermatitis, previously published in peer reviewed journals were used. Critical appraisal of included studies was performed using the Mixed Methods Appraisal Tool. Data were extracted and thematically synthesized to generate descriptive and analytical themes. The confidence of the findings of the included studies was assessed via either GRADE or CERQual. Twenty-three studies were included. Findings showed that community pharmacists lacked knowledge of the uses of topical corticosteroids. The recommendations of other treatments were limited. Pharmacists generally undertook dermatology training after graduation. Analytical themes indicated that the practices of community pharmacists were poor and misled patients. Inappropriate education in initial training was identified as a potential reason for their poor practices. This systematic review reveals a gap between patients’ needs in practice and dermatological education provided to community pharmacists. Novel approaches regarding education and training should be explored to improve pharmacists’ dermatological knowledge and skills.


Introduction
Atopic dermatitis (AD), which is also known as atopic eczema, is a skin disorder with a prevalence rate of 15-20% in developed countries [1]. It is usually accompanied by allergic rhinitis, asthma, and infection [2]. Although typically regarded as a childhood disease that presents before children reach one year of age, with the highest prevalence of onset being in 0-6-month-old infants [3], some patients (10-30%) may still have symptoms during adulthood [4]. AD is generally characterized by inflammatory flare-ups accompanied by acute (reddish and swollen) or chronic (lichenified) pruritic lesions on the skin [5]. According to streamlined and validated diagnostic criteria devised by the American Academy of Dermatology (AAD), essential features, such as pruritus, must be present for diagnosis. Some important features, such as an early age of onset, also support the diagnosis [6]. The clinical severity of AD is assessed based on the affected area and intensity using a standardized SCORAD tool [7]. As a recurrent chronic condition, AD affects patients' physical health, financial circumstances, and quality of life [8].
Moisturizers are the mainstay of ongoing management of AD, and topical corticosteroids (TCs) are the first-line treatment for inflammatory symptoms and flare-ups. Topical

Search Strategy
The review followed PRISMA [26] guidelines and was registered with PROSPERO (CRD42022308405). The search strategy, which is explained in the Supplementary Material document (Table S1), identified studies that investigated practices and perceptions of community pharmacists regarding the management of AD. Five databases (Ovid MED-LINE, Ovid EMBASE, EBSCO Cumulative Index to Nursing and Allied Health Literature (CINAHL), PsycINFO, and PubMed) were searched for data collected between their date of inception and December 2022. The search strategy was developed by the primary author (ABC), reviewed by other authors (LL, APR), and quality checked by a specialist librarian.

Selection Process and Inclusion Criteria
After the search, all identified articles were sent to Endnote. All titles and abstracts were reviewed by ABC to determine their eligibility. All authors assessed these titles against the inclusion criteria, which were determined in line with PICOS (population, intervention, control, outcome, and study design), as shown in Table 1. Inclusion criteria for studies were as follows: (i) research available in full-text form, (ii) primary research discussed in any language, (iii) research published in peer-reviewed journals, and (iv) research that investigated practices and perceptions of community pharmacists regarding the management of AD. Studies that did not fulfil the inclusion criteria were excluded.

Assessment of Methodological Quality
The methodological quality of the studies was appraised by ABC using the Mixed Methods Appraisal Tool (MMAT) [27] and reviewed by the remaining authors (LL, APR). Disagreements were solved via discussion. MMAT was used as it enables quantitative, qualitative, and mixed method studies to be critically appraised [28]. After two screening questions were asked, five questions remained, which participants could answer with either "yes", "no", or "can't tell" responses. The results gave an overall assessment of methodological quality using either 0-1 (low quality), 2-3 (medium quality), or 4-5 (high quality) scores.

Data Extraction and Synthesis
Information (author and year, country, study design, methods of data collection, participants, number of participants, aim, key findings, and further recommendations of study) was extracted from the involved studies by ABC and reviewed by APR and LL. Data from qualitative and quantitative studies were synthesized using thematic synthesis [29], and a data-based convergent integration approach was applied [25]. Firstly, the quantitative data were subjected to a process known as "qualitizing" or "data transformation", in which quantitative results were turned into textualized qualitative data [30,31]. This process was carried out by ABC, who converted summaries of statistical responses and author commentaries into descriptive textual data, which were then checked by APR and LL to synthetise quantitative data alongside the qualitative findings. Afterwards, the qualitized data and qualitative findings were synthesized via the following three-stage approach: (1) inductive line-by-line coding of findings acquired from themes, quotes, and author commentaries in qualitative studies and descriptive textual data in quantitative and mixed methods studies, as well as author commentaries; (2) combination of related codes into "descriptive" themes; and (3) generation of "analytical" themes based on the interpretation of the findings that went beyond the primary findings [29]. Initial coding and identification of descriptive themes were performed by ABC and reviewed by APR and LL. The agreed descriptive themes were combined into analytical themes through discussion until consensus was achieved among all authors.

Assessment of Confidence
The confidence of the synthesized findings obtained using qualitized descriptive quantitative and qualitative data was evaluated via the Confidence in the Evidence from Reviews of Qualitative Research (CERQual) tool [32], and findings derived from pre-and post-education intervention studies were assessed using the Grading of Recommendations Assessment, Development, and Evaluation (GRADE) approach [33]. The confidence was assessed using the CERQual tool based on four components-methodological limitations of the included studies, the relevance of included studies to the review question, the coherence of the findings, and the adequacy of the data used to support the review finding-and the GRADE tool was used to evaluate the following criteria: risk of bias, imprecision, inconsistency, indirectness, and magnitude of effect. Both tools judged the quality of evidence using "high", "moderate", "low", or "very low" rankings.

Outcomes Assessed
The main outcomes assessed to examine practices and perceptions of community pharmacists were their knowledge, recommendations, attitudes, and experiences regarding the management of AD. Secondary outcomes included the perspectives of other individuals (healthcare providers, patients, and parents) on pharmacists' practices.

Results
A total of 6657 articles were identified. After removing duplicates and completing the screening stage, 100 studies remained and were evaluated for eligibility, and 80 studies were excluded. A further three studies were identified by searching the references of included studies. Finally, 23 studies (Figure 1), which were all published in English, except for one study published in Japanese, which was translated by a translator, between 1995 and 2021, were included for analysis.
The results of quality assessment are shown in Table S2. There was much diversity in scores across studies, which ranged between low and high quality. Only one study was denoted as being of low quality [56]. The quality scores of the quantitative studies ranged from low to high quality, with 13 of 18 studies ranked as being of medium quality. All qualitative studies were ranked as being of high quality [35,42,45]. Two mixed methods studies were rated as being of medium quality [36,38]. Common issues related to study quality and risk of bias for quantitative and mixed methods studies were unclear descriptions of the target population and the sample, as well as well-described inclusion and exclusion criteria for the sample. The main issue that affected qualitative and mixed methods studies was a lack of clarity regarding the way in which the findings were derived from the data.

Descriptive Themes
Synthesized statements derived from descriptive quantitative and qualitative data were produced, and the confidence level of each statement was assessed using the CERQual tool (see Table S3). Other statements from pre-and post-intervention studies were evaluated using GRADE. As the designs of experimental intervention studies were evaluated as poor, the general rating of findings was reduced from low to very low quality [57]. Two descriptive themes and their sub-themes were identified via the analysis by combining relevant codes ( Most studies (n = 19) were conducted in OECD countries: six studies were conduc in the United Kingdom [34][35][36][37][38][39]; two studies were conducted in each of Australia [40,  using GRADE. As the designs of experimental intervention studies w uated as poor, the general rating of findings was reduced from low to very low [57]. Two descriptive themes and their sub-themes were identified via the analysis bining relevant codes ( Figure 2; Theme 1: Current Practice and Theme 2: Impact macists). The descriptive themes and sub-themes are outlined below.

Knowledge of Corticosteroids and Other Treatments
Knowledge of corticosteroids was a significant theme, having FTU-and ph corticophobia-related sub-themes, and it was mentioned in 14 studies [36, Pharmacists were shown to lack knowledge of TC potency in the literature (C high) [36,53,54]. Poor knowledge regarding the length of TC use was also reporte Qual-moderate) [48,49,51,54].
Fingertip unit (FTU): Most pharmacists did not use standard measures, such as FTU, to communicate dosing instructions to patients in the literature. Instead, the literature indicated that patients were told to apply doses thinly (CERQual-moderate) [42,48,54]. Two more studies also stated that a tiny minority of pharmacists recommended FTU to patients (CERQual-moderate) [47,51].
Similarly, pharmacists tended to tell patients to "apply it sparingly" in Australia, though they began using FTU after an educational intervention (GRADE-very low) [41]. It was also found that although most pharmacists knew the amount that can be measured via FTU, only the minority of them often or always advised patients to use this method (CERQual-moderate) [36,47].
Other treatments, including emollients, lifestyle habit changes, TCIs, and CAMs, were also mentioned [36,42,44,46,54,55]. Regarding emollients, most pharmacists recommended using them as an initial treatment (CERQual-moderate) [36,54], even if they were not prescribed by doctors (CERQual-low) [42], and patients were advised by pharmacists to use them regularly for a prolonged period (CERQual-low) [36]. CAM use was mentioned in only one study [55] and CAMs were seen as more comprehensive and beneficial treatments than current treatment by some pharmacists (CERQual-low). Recommendation of TCI use was mentioned in one study, in which pharmacists explained that a tingling sensation is a common side effect about which patients should not worry (CERQual-low) [46]. Another study noted that pharmacists rarely gave recommendations about lifestyle habits to patients (CERQual-low) [42].

ii. The Frequency and Diagnosis of Atopic Dermatitis in Pharmacies
AD is one of the most prevalent skin conditions seen in pharmacies (CERQualmoderate) [37,39,40,48]. Community pharmacists carry out more medicine reviews for eczema than any other skin condition in the UK (CERQual-low) [39].
Two studies evaluated the diagnostic ability of pharmacists using expert assessors [38,40]. Although some assessors concurred with the diagnoses determined by pharmacists, medical history-recording behaviors of pharmacists were found to be inadequate (CERQuallow) [38]. Furthermore, only in 67% of cases diagnosed as AD did a dermatologist agree with a pharmacist's decision (CERQual-low) [40].

iii. Continuing Training for Pharmacists
Many studies demonstrated that pharmacists often continued their dermatology education after graduation (CERQual-moderate) [36,37,39,40,49,52,53,55]. Pharmacists were eager to expand their dermatological expertise, which they acquired by joining educational programs or training sessions held by drug manufacturers, attending conferences and branch meetings, or reading journal articles and e-bulletins (CERQual-moderate) [35][36][37]49]. There was a strong correlation between the extent to which continuing their training in dermatology helped pharmacists and their overall self-confidence (CERQual-low) [39]. Pharmacists who undertook continued dermatology training displayed better knowledge, attitude, and practices regarding TC treatment (CERQual-moderate) [53].
Counseling services by pharmacists were also reported [34,37,38,43,44,52,56], and most patients were satisfied with the service (GRADE-very low) [34,43], as were pharmacists (GRADE-very low) [44]. However, in a study conducted in Iraq, most patients did not receive any information about the use and adverse effects of TCs from pharmacists (CERQual-very low) [56].
Patient privacy was not usually a concern for pharmacists [41,45]. Pharmacists held consultations with patients in front of other people (GRADE-very low) [41], and patients reported feeling agitated during the consultation [45]. Furthermore, patients reported that pharmacists were not able to understand patients' circumstances (CERQual-low) [45].
ii. Inter-professional Communication In the literature, communication and collaboration between pharmacists and healthcare professionals was weak (CERQual-moderate) [35,45,49,50]. For example, different guidelines were used by healthcare professionals, with no synchronized approach used, and this issue may cause confusion for patients (CERQual-low) [35]. Moreover, the duration of use of TCs prescribed by physicians was mostly decreased by pharmacists after plausibility checks (CERQual-moderate) [49,50].

Analytical Themes
Through the analysis of descriptive themes, two analytical themes were determined, which sought to go beyond the findings reported in the original study [58]. The analytical themes discovered were "misleading position" and "perceptions of education and training".

Misleading Position
Pharmacists potentially misinformed patients regarding knowledge of and recommendations and practices regarding AD and its treatment. Although AD was a skin condition commonly seen in pharmacies, while community pharmacists considered themselves to be first-line providers of treatment to patients with dermatologic conditions (Quote 1), they may misinform patients using TCs because of their insufficient knowledge about the potency of TCs (Quote 2).
"Pharmacists should be the first port of call for patients with a skin problem". [37] Quote 1 "In terms of formulations, over 60% did not know how many topical corticosteroid potency categories exist". [36] Quote 2 Besides insufficient knowledge of TCs, pharmacists lacked a standardized way of communicating advice to patients who used topical treatments. Rather than using FTU, they recommended thinly applying topical medications (Quote 3).
"Of course, you have those fingertip units. Well, I must confess that we don't really work with it to indicate how much you have to apply. We just say: apply thin. It is still a hormone cream". [42] Quote 3 (Pharmacist) Moreover, different terms, besides "applying thinly", were used by pharmacists, which may make patients more confused and worsen existing corticophobia. Subsequently, this situation may result in treatment non-adherence.
"When directing the amount of TCS to be applied, 54% reported informing the patient that TCS should be used sparingly. . ." [41] Quote 4 Despite AD being one of the most commonly encountered conditions in pharmacies, the pharmacists' ability to record medical histories in some cases was poor (Quote 5). This issue may lead to patients being misinformed about the proper use of treatment or cause misdiagnosis.
"A more detailed history would have been helpful and may have supported making the diagnosis". Regarding emollients, although pharmacists advised patients to apply emollients, even if they were not prescribed (Quote 6), they did not take into consideration the utility of tailored moisturizers for different skin types, sensitivities, or allergies. "Maybe they weren't told about the emollient at the GP. And then you give the advice to use a moisturizer. . ." [42] Quote 6 (Pharmacist) Overall, with moderate-to-high confidence, the evidence suggests that pharmacists were misinforming patients about AD management in practice. With lower confidence, findings also suggested poor diagnosis by pharmacists. Therefore, we can conclude with moderate confidence that community pharmacists may inadvertently play a role in patients being misdiagnosed, inaccurately using treatment, or using an insufficient amount of medicine.

Perceptions of Education and Training
The literature showed that pharmacists received postgraduate training in dermatology, and most appeared to be satisfied with these educational tools. Besides training, pharmacists and their teams used educational interventions for the treatment of AD, which helped them to improve their treatment practices (Quote 7,8).
"Of those (pharmacists) surveyed, 92% stated they would advise TCS be used until the eczema is clear, compared to 27% prior to education (p < 0.0001)". Considering the educational level of community pharmacists regarding dermatology, further educational training is perceived as effective at improving practice and patient care. However, in the literature, current practice of pharmacists was poor, which may be caused by the fact that knowledge acquired via initial education alone might not be enough to ensure good quality care in practice. Hence, the gap between pharmacists' knowledge and the needs of the patients can be addressed by improving dermatological education in the initial training of pharmacists.
Overall, with moderate confidence, the evidence showed that pharmacists were willing to extend their knowledge through further education, though the confidence of findings regarding the effectiveness of educational interventions was very low.

Summary of Findings
This study reviewed the literature regarding the practices and perceptions of community pharmacists in the management of AD. A key treatment recommended by pharmacists was TCs, though only a few studies mentioned their knowledge and practices regarding other treatments. The most striking finding to emerge from the analysis is that pharmacists did not effectively communicate information about TCs to patients. Pharmacists lacked knowledge of TC practice and duration of treatment. In addition, they had corticophobia. Although most pharmacists knew about FTU, they did not use it. Even though "apply thin" has been removed from labels and the FTU has been promoted in the Netherlands since 2013 [59], this practice was retained by pharmacists in 2019 [42].
Regarding corticophobia, some pharmacists exhibited more fear of using TCs than other healthcare professionals, and this situation encouraged patients to be suspicious of TCs. A key finding is that a pharmacist's stance on TCs may mislead patients regarding their effective use and treatment. A similar position was offered by Smith et al., who reported that cautious approach preferred by pharmacists may encourage patients to avoid TCs [60]. Subsequently, this situation may lead to the ineffectiveness of therapy, since corticophobia is already quite high in patients with AD from 15 different countries [61] and seen as one of the main reasons for non-adherence [16]. It cannot be denied that corticophobia is common in patients; however, it is important for pharmacists to provide accurate and unbiased information and support to patients with AD.
Another key finding is that pharmacists could provide better AD support in practice if they received more comprehensive education on dermatology. It was shown that the counseling practice of community pharmacists was affected by their level of education [62]. This finding is supported by a previous study, which found that re-education of pharmacists was a potential way to enhance confidence in the treatment provided [60], especially as the ability to address dermatological questions has been found to be low among pharmacy students [63]. In addition, receiving educational training was linked to confidence in dealing with skin conditions [64]. Furthermore, an e-learning educational program that included corticophobia and FTU sections was implemented in a past study, and an increase in the knowledge of AD management was observed in pharmacists [65].

Implications for Practice and Policy
While community pharmacists play a key role in counseling patients with AD, they lacked practical knowledge of the management of the condition. Pharmacists could negatively influence patients by advising incorrect ways of using topical treatments, preventing proper use of TCs and potentially causing misdiagnosis of conditions. The findings also showed that pharmacists attended a range of training courses related to dermatology after graduation. There is an evident gap between patient needs in pharmacy practice and initial education. This gap can potentially be reduced via educational interventions, such as giving pharmacy students sufficient knowledge of the use of TCs and other topical treatments and providing more comprehensive competency-based practice education regarding dermatology. If patients are not appropriately helped to manage their condition by pharmacists, they may continue their usual routine, and the condition may remain unmanaged. An increase in the number of unmanaged AD patients may put more financial burden on countries' health systems, since AD has a significant financial effect on health care systems [66]. To avoid this burden, preventative action can be taken by policymakers and academics. Providing dermatological training during initial pharmacy education should help pharmacists to develop the improved knowledge and skills required to meet patients' needs in practice. This training should draw on expertise from dermatologists, patient experts, and practices that are captured in current guidance [23,67,68]. This training needs to be ongoing and embedded in practice through continuous professional development to ensure that pharmacists can appropriately assess, diagnose, prescribe, and monitor AD, as well as communicate with patients, in community pharmacy settings.

Strengths and Limitations of the Study
The strength of the study is that it identified, for the first time, the current strengths and weaknesses of the practices used by pharmacists to supporting patients with AD. Regarding limitations, TC was the most commonly mentioned medication in this review, though it does not give a full picture of counseling practices used by pharmacists for all treatment options. Some studies notably concentrated on paediatric eczema, though eczema is not seen in children alone. Some included studies discussed other skin conditions besides AD, and this issue may limit these studies' findings' of relevance to AD. In addition, all studies were derived from either OECD, GCC, or less developed countries; thus, the findings of this study may not be applicable to least developed countries. Some studies cited other healthcare professionals as well as pharmacists, and it was possible to separate the findings attributed to pharmacists in these studies. However, in two studies [43,44], pharmacists and technicians, and in one study, [46] community and hospital pharmacists were grouped together as pharmacy staff, meaning that distinguishing the pharmacists' contributions was not possible in these studies.

Further Research
Further studies are needed to broaden this topic's focus to cover other treatments of AD, rather than only studying TCs. The focus of future pedagogical research needs to be on establishing steps that can be taken as part of initial education to improve practice of future pharmacists in supporting patients with AD. Based on the low confidence rates presented in some studies, more robust research is needed. There is also a gap in evidence regarding pharmacist management of AD in least developed countries.

Conclusions
The purpose of the study was to examine community pharmacists' contribution to the management of AD. This study has shown a gap between community pharmacy practice and pharmacists' training and education. This gap means that pharmacists inadvertently mislead patients in practice by reinforcing fear of TC use and providing inadequate counseling about the duration and application of topical treatment. Despite significant receiving undergraduate and postgraduate training, the literature indicates that community pharmacists lacked the knowledge and skills required to effectively respond to the needs of AD patients in practice, encouraging them to seek further dermatology training to make up for the educational deficiency of their initial training. The findings of this research provide insights into the gap between practice and education, showing that novel educational interventions are required to improve AD management.
Supplementary Materials: The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/healthcare11152159/s1, Table S1: Detailed search strategy; Table S2: Quality assessment of included studies; Table S3: CERQual full evidence profile; File S1: PRISMA 2020 checklist. Refs [26,   Acknowledgments: This work was conducted as a part of a doctoral study, supported and funded by the Ministry of National Education of the Republic of Türkiye.

Conflicts of Interest:
The authors declare no conflict of interest.  Pharmacists who received educational training had better questionnaire scores than those who did not receive training. • There were knowledge, attitude, and practice differences between those who graduated from international and local institutions.

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There was low score in terms of use of potent corticosteroid in cases of acute flare ups of eczema.

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Many pharmacists thought that corticosteroids should not be used in children.
• Proper courses regarding the appropriate use of corticosteroids should be integrated into the curriculum to educate pharmacists. • Pharmacists mainly explained the best application site to patients regarding use of corticosteroids if they were using it first time, and pharmacists' knowledge of guidelines positively affected their recommendations.

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Pharmacists urged patients to apply topical medications until their situation improved.

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Pharmacists gave information about tingling effects associated with the use of calcineurin inhibitors and told patients that this issue is common side effect. However, this approach caused anxiety in some patients.

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Pharmacists complained that doctors' instructions regarding the frequency and site of application were not clear.
To effectively counsel eczema patients, pharmacists should be aware of treatment guidelines for AD and are urged to follow these guidelines.     Pharmacists mostly found postgraduate training to be helpful in terms of dealing with patient requests, and this willingness was positively associated with overall self-confidence.
Further studies should be conducted to identify whether these reviews contribute to better disease-related outcomes. • Pharmacists' diagnoses were evaluated by assessors and found to be accurate in over a third of cases (34%). However, assessors' rate of disagreement with pharmacists' diagnoses was higher. In addition, assessors found the questioning and medica history-recording practices of pharmacists to be inadequate.

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Pharmacists' approaches to treatment were accurate in almost half of all cases. • Over half of patients felt that their skin problem had been completely resolved through the treatment provided at the pharmacy.
Patient assessment-related education for pharmacists should be considered, with particuar focus on dermatology.