Background

The development of antimicrobials has been one of the most significant events in modern medicine over the past century [1]. However, their indiscriminate use has become a growing public health concern as antimicrobials have been strongly implicated in the development of microbial resistance [2, 3]. Globally, microbial resistance is responsible for an estimated 700,000 deaths per year, which could increase to as much as 10 million by 2050 if this problem is not addressed [4, 5]. In the United States, microbial resistance has caused an estimated two million infections and 23,000 deaths, with an annual economic impact of US$ 55–70 billion [6].

In this context, health systems worldwide face the challenge of addressing microbial resistance. According to the World Health Organization, approximately 93% of access to antimicrobials comes from community pharmacies [7]. From this perspective, pharmacists can be considered the last barrier during the dispensing process, capable of preventing inappropriate use of antimicrobials and the possible health problems that could result from such use [8]. The dispensing has wide visibility in community pharmacies, is highly accessible, and serves many patients seeking treatment-related counseling and medicine [9].

Drug dispensing is a service that ensures the provision of medicines and other health products through analysis of the technical and legal aspects of a prescription, assessment of individual health needs, and medical intervention through pharmaceutical counseling and documentation [10, 11]. A well-structured dispensing process can become a valuable service because it can limit indiscriminate antimicrobial use, and therefore, microbial resistance [12].

Studies have indicated that interaction between pharmacists and patients enables interventions that optimize the use of antimicrobials in community pharmacies [13]. Despite this, there is little scientific evidence on the panorama of antimicrobial dispensing practices and interventions provided by pharmacists. Previous studies have focused on the frequency and proportion of the sale of antimicrobials without prescriptions in community pharmacies, and the main diseases, and antimicrobials involved in these practices [13,14,15], as well as pharmacists’ perceptions of antimicrobial sales without prescription [8, 16].

Thus, there remains a gap in the way this service is provided to patients, with little emphasis placed on the dispensing process; in other words, how the dispensing service has been provided to patients and what pharmacist interventions have been carried out during this service. Therefore, exploring pharmacist interventions will optimization of the antimicrobial dispensing service, and development of strategies that mitigate the burden of microbial resistance and its impacts on society.

Hence, studying antimicrobial dispensing processes in community pharmacies worldwide is important. An understanding of the behaviors, counseling, and interventions provided by pharmacists during antimicrobial dispensing, will help to develop strategies that address the gaps in this service and improve the dispensing process in community pharmacies. Therefore, this study aimed to determine the antimicrobial dispensing process in community pharmacies.

Methods

Study design

This scoping review adopted the methodology described in the Joanna Briggs Institute Reviewer’s Manual [17] and was based on the Preferred Reporting Items for Systematic Reviews and Meta-Analyses extension for scoping reviews (PRISMA-ScR) criteria [18]. Scoping Review was performed as the objective of the present study was to map, or identify, the available literature related to the process of dispensing antimicrobials [19].

Identification and development of research questions

As this review mainly focused on the antimicrobial dispensing process, the research question was “what are the antimicrobial dispensing processes in community pharmacies?” Based on this research question, five areas of interest were identified.

  • RQ1: What are the most frequently dispensed classes of antimicrobials?

  • RQ2: What are the methods used to evaluate antimicrobial dispensing?

  • RQ3: What is the main counseling provided to patients by pharmacists and the pharmacy team during antimicrobial dispensing?

  • RQ4: What are the others interventions performed by pharmacists and the pharmacy team for patients during antimicrobial dispensing?

  • RQ5: How do studies assess the quality of antimicrobial dispensing?

Search strategy

A literature search was performed in September 2020 using the following databases: PubMed/MEDLINE, LILACS, Cochrane, Web of Science, and Embase. The search strategies were drafted according to a database protocol using search terms related to dispensing, anti-bacterial agents, and pharmacies and their combinations. The search strategy employed both standardized terms from the controlled vocabulary of the “National Library of Medicines” through the “Medical Subject Headings (MESH)” and non-standard terms to extend the search. The “All fields” search option was used. No date limit was used in the database search and relevant studies published up to September 2020 were identified. The full search is available in the Additional file 1.

Study selection

Two reviewers (E.V.S. and L.J.S.C.V.) independently screened the search results using the Rayyan tool (http://rayyan.qcri.org) [20], and identified potentially relevant studies based on their titles and abstracts. Relevant studies were read in full and selected according to the eligibility criteria. Disagreements between the two reviewers were resolved by a third reviewer (S.C.S.).

Eligibility criteria

The study selection criteria were established according to the population-concept-context framework, as recommended by the Joanna Briggs Institute for scoping reviews [17]:

  • Population: community pharmacists and pharmacy team

  • Concept: antimicrobial dispensing process

  • Context: community pharmacy

Inclusion criteria

Studies that met the following criteria were included: (i) original articles; (ii) studies published in English, Portuguese, and Spanish; (iii) studies exploring antimicrobial dispensing processes; (iv) studies performed in community pharmacies; (v) studies that evaluated interventions during dispensing; and (vi) studies with pharmacists and pharmacy team as participants. No limitations were applied in terms of the publication year or study design.

Exclusion criteria

The following studies were excluded: (i) academic documents such as theses and dissertations; (ii) studies without full text available; (iii) meta-analyses, systematic reviews, narrative reviews, letters, editorials, commentaries, posters, and conference proceedings; and (iv) studies in which separating antimicrobial dispensing data from those of other drug classes was not possible.

Data extraction

A standardized data graph form was created, and data extraction was performed in duplicate. The initial categories included general study characteristics such as authors, year of publication, country, study objective, study design, and sample. Information was collected on antimicrobial dispensing practices, including antimicrobial dispensing with and without prescription, methods for evaluating the dispensing of antimicrobials and assessing the quality of dispensing, classes of antimicrobials dispensed/studied, and limitations. In the present study, evaluation of dispensing quality focused on the instruments or quality indicators used by the studies that reported minimal counseling or other interventions provided by pharmacists for the rational use of medicines.

Analysis and presentation of the results

The findings were presented in a descriptive form. Figures and tables were used as appropriate to illustrate or summarize the key findings.

Results

Search results

A total of 4887 articles were identified during the initial search. After excluding duplicates (n = 2826) and irrelevant articles based on the titles and abstracts (n = 4760), 127 potentially relevant articles were retrieved for full-text evaluation. Of these, 35 met the inclusion criteria and were included in the scoping review [21,22,23,24,25,26,27,28,29,30,31,32,33,34,35,36,37,38,39,40,41,42,43,44,45,46,47,48,49,50,51,52,53,54,55] (Fig. 1).

Fig. 1
figure 1

Flow diagram of literature search and screening process

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Characteristics of the selected studies

A description of the general characteristics of the 35 included studies is provided in Table 1. These studies were published between 2006 and 2020, and 22 (63%) were conducted in Asia, 7 (20%) in Africa, 4 (11%) in Europe, 1 (3%) in North America, and 1 (3%) in South America. Regarding study design, 31 studies were cross-sectional, 3 were qualitative, and 1 used more than one study design (mixed methods). Moreover, 31 (89%) studies investigated the practice of antimicrobial dispensing/sales without prescription, and only four (11%) studies evaluated the same with prescriptions. We did not observe any difference in the antimicrobial dispensing process with or without prescriptions.

Table 1 Characteristics of the selected studies
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Classes of antimicrobials most often dispensed/studied

Among the classes of antimicrobials most addressed by the studies, were penicillins (n = 54; 33.1%), with amoxicillin and amoxicillin + clavulanate being the most recurring regimens, followed by macrolides (n = 26; 15.9%), cephalosporins (n = 25; 15.3%), quinolones (n = 25; 15.3%), lincosamides (n = 9; 5.5%), aminoglycosides (n = 6; 3.7%), tetracyclines (n = 6; 3.7%), sulfonamides (n = 6; 3.7%), and others (n = 6; 3.7%) (Table 2).

Table 2 Antimicrobials dispensing practices of studies
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Methods used to evaluate antimicrobial dispensing process

Of the 35 studies included in this review, 22 (63%) used the simulated patient method to evaluate antimicrobial dispensing and 13 (37%) used face-to-face interviews, questionnaires, and pharmacist documentation methods (Table 2). In studies that used the simulated patient method, the main scenarios were related to the following health conditions: sore throat, diarrhea, respiratory tract infection, urinary tract infection, and otitis media. The study samples were heterogeneous and varied from 6 to 2,411 community pharmacies and 98 to 202 pharmacists.

Antimicrobial dispensing process

Regarding dispensing antimicrobials, community pharmacists and pharmacy team asked questions more frequently than provide counseling or other interventions. Of the 35 studies, the most frequently asked questions were about drug allergies (n = 19, 54.3%), patient symptoms (n = 18, 51.4%), and the use of other medicines (n = 13, 37.1%). The main counseling provided by community pharmacists was about the side effects (n = 14, 40%), and precautions (n = 14, 40%), how to take the medicine (n = 12, 34.3%), and duration of medication (n = 11, 31.4%). In addition, seven other interventions were performed, of which referral was the most common (n = 15, 42.8%), followed by refusal to dispense antimicrobials without prescription (n = 12, 34.3%) (Table 2).

The process of dispensing antimicrobials in clinical cases is presented in Table 3. It was observed that for most cases, the pharmacists asked about patient symptoms, of which cough (78%) and common cold (51%) were the most common. Among clinical cases, counseling on how to take the medicine was most frequent in cases of urinary tract infection (51%) and otitis media (50%), followed by how long the medication should be taken in cases of urinary tract infection (42%) and otitis media (40%). Regarding other interventions, the most frequent was referrals, with the highest frequencies for acute sinusitis (26%) and otitis media (23%). Of note, no study reported the evaluation of antimicrobial dispensing quality.

Table 3 Practices of antimicrobials dispensing for clinical cases
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Discussion

Despite extensive literature on antimicrobial dispensing, most studies have focused on dispensing antimicrobials without prescriptions. This is especially true in the low- and middle-income countries in Asia and Africa. Corroborating these data, a systematic review by Batista et al. [16] identified that the highest percentage of dispensing antimicrobials without prescription occurred in Asia. Among the main factors that contribute to this practice are the unavailability and inaccessibility of health facilities, economic benefits to the pharmacy team, limited knowledge of antimicrobials among the population and pharmacy team, lack of information about the negative impact of this practice, and ineffectively imposed regulations [16, 56,57,58]. Therefore, multifaceted strategies should be developed to address these problems, including population awareness and professional qualifications, to reduce inappropriate antimicrobial use.

Most of the studies included in this review used the simulated patient method to assess the antimicrobial dispensing process. The simulated patient method consists of the visit of a trained individual to the pharmacy, indistinguishable from a genuine patient, who enacts predetermined scenarios, to assess information gathering and counseling provided by pharmacists in the supply of medicines. Simulated patient methods provide an unobtrusive means of observing actual practice behavior and are considered the ‘gold standard’ for the measurement of the quality of behavior [59,60,61]. Furthermore, this method has considerable advantages over other methods for assessing service quality as it minimizes the Hawthorne effect [59]. Thus, studies should use the simulated patient method to assess the care provided by pharmacists and promote a change in practice.

In the present study, pharmacists and pharmacy team asking more questions than provided counseling on medicine use. Other studies have also shown low percentages of counseling provided by pharmacists and pharmacy team [16, 51]. The literature agrees that pharmaceutical counseling is an essential component of dispensing [11, 62, 63]. The counseling provided by pharmacists during dispensing not only reduces inappropriate use of antimicrobials but also improves treatment adherence and increases patient awareness of the importance of the treatment regimen [64]. Therefore, although certain factors can influence the quantity and quality of pharmaceutical counseling, this intervention must always exist in the drug dispensing.

Among the included studies, medical referral was another intervention performed to encourage patients to attend primary healthcare units. Likewise, a study by Chang et al. [51] also noted that in some cases, referrals were recommended instead of dispensing antimicrobials without prescription. Other studies have reported low rates of intervention and interest in patient health needs [42, 65]. Chowdhury et al. [52] conducted educational interventions aimed at controlling the indiscriminate sale of antimicrobials; the interventions led to fewer referrals and only reduced the dispensing of antimicrobials for children. This evidence raises concerns regarding the attitude adopted by pharmacists and pharmacy teams, as medical referrals can potentially reduce the development of microbial resistance owing to the indiscriminate use of antimicrobials for health conditions that do not require such treatment. Thus, there is an urgent need to encourage a proactive attitude among pharmacists and to combine educational interventions by the pharmacy team and raising awareness about proper antimicrobial use among the general population.

This scoping review revealed that no study has assessed the quality of the antimicrobial dispensing process thus far, highlighting an unmet need. Previous studies have used methods to assess dispensing processes, such as the use of instruments available in the literature [65] and performance assessment sheets constructed by the authors based on guidelines and observation protocols by the authors [66]. Although the identification and measurement of quality services is challenging, quality assessment is imperative to identify problems, deficiencies in the provision of care, and points of improvement, and to delineate strategies to overcome these deficiencies and monitor the effectiveness of corrective measures [67]. Therefore, future studies should invest in the development of quality indicators for antimicrobial dispensing and the development and validation of instruments to assess the quality of dispensing. We also recommend that future studies be conducted to provide evidence for the quality of the antimicrobial dispensing process.

In low- and middle-income countries, we noted that properly trained pharmacists and pharmacy team could be a part of the solution to overcome this global challenge of microbial resistance, and we emphasize that training can improve the role of pharmacy professionals [68]. These issues reinforce the need for pharmacists to continue their education while working in community pharmacies. Our findings highlight the urgency for policymakers to develop multifaceted approaches to qualify for the practice of dispensing antimicrobials. Therefore, there is a need for a patient-focused approach that minimizes the sale of these medicines without prescription.

To address the problem of the indiscriminate use of antimicrobials, multifaceted strategies, including implementing educational and/or regulatory/administrative measurements, promoting changes in cultural practices, and adopting advertising resources with the potential for reinforcement and perpetuation of information that aims educate the population about the risks regarding the indiscriminate use of this class of medicines. Moreover, dispensing practice should be regulated, as it has the potential to mitigate the irrational use of antimicrobials and reduce microbial resistance, in view of the strategic position occupied by community pharmacists and pharmacy teams.

Strengths and limitations

To the best of our knowledge, this scoping review is the first to map and analyze, in the current literature, the range of studies that investigated the dispensing of antimicrobials with and without prescriptions, with a focus on pharmacist interventions. Hence, this study did not use backward or forward snowballing to identify additional relevant studies. There was heterogeneity in the study design, sample, and methods; thus, caution should be exercised when generalizing the results to other health conditions and specific patient populations.

Conclusion

Antimicrobial dispensing processes have mainly been investigated in low- and middle-income countries, with a focus on dispensing antimicrobials without prescriptions. Minimal questions were asked, and patient counseling was below the levels expected of pharmacists and pharmacy team during the dispensing process, identifying a deficiency in the practice. Therefore, improving antimicrobial dispensing processes to promote the rational use of these medicines is necessary. Furthermore, stakeholders should develop multi-faceted strategies to mitigate microbial resistance.