Evaluation of the perspective of pharmacists on antimicrobial stewardship and the barriers to its consolidation in hospitals: a cross-sectional study

Abstract

Antimicrobial Stewardship Programs (ASPs) are associated with positive outcomes, but seem to be consolidated in few hospitals. This study aimed to evaluate ASPs in Brazilian hospitals and the barriers to their consolidation from the pharmacists’ perspective. This is a cross-sectional study. Data were collected through an online questionnaire applied to hospital pharmacists. Data analysis was performed by descriptive statistics and Spearman's ordinal correlation test. A total of 83 pharmacists participated in the study and 45.8% stated that the hospital in which they worked had an ASP. The ASPs were predominantly implemented in public hospitals, with a greater number of beds in the intensive care unit and beds in general. The main barriers to the consolidation of ASPs were: reduced number of pharmacists, time allocated to other demands of the pharmacy, the ineffectiveness of the communication process with doctors, and lack of access to reliable information about antimicrobials in the hospital. Pharmacists that work in hospitals where ASPs were implemented were more confident (p = 0.000) and with a better perception of the barriers that prevent their consolidation (p = 0.003. The ASP was commonly adopted in public hospitals with a greater number of beds. The main obstacles to consolidation were infrastructure, economic, and educational resources.

Introduction

Antimicrobials are among the most prescribed drugs in hospitals. However, their indiscriminate use is directly related to increased mortality, morbidity, length of stay, and healthcare costs [1]. In a Canadian study, one in five emergency room visits were due to adverse events related to these drugs [2]. In addition, around 30% to 60% of the antimicrobials used in the Intensive Care Unit (ICU) are dispensable, inappropriate, and sub-optimal [3, 4]. But certainly one of the main problems that is specifically associated with the inappropriate use of this type of medication is antimicrobial resistance (AMR), with data that proves inadequate use and contributes to unsatisfactory clinical outcomes.

The Center for Disease Control and Prevention (CDC) estimates that in the USA there are 2.8 million infections a year caused by resistant microorganisms, which result in more than 35,000 deaths [5, 6]. At a global level, it is estimated that AMR causes 700,000 deaths a year, with a predicted increase to 10 million by 2050, along with economic crises [7]. In addition to these facts, it has to be considered that the development of new drugs that are effective against drug resistant bacteria has not kept pace with the phenomenon of multidrug resistance. It is believed that without effective action to change the way antibiotics are used, the world will continue to move towards a post-antibiotic era, in which there will be no antibiotics to treat simple infections caused by multidrug-resistant bacteria [8]. The prevention of AMR is one of the pillars of the fight against serious infections, and it is essential to understand the phenomenon of increasing AMR, especially in critical healthcare environments such as the ICU, due to the significant impact on clinical, microbiological and financial areas [3, 4].

In this context, the Antimicrobial Stewardship Program (ASP) emerges as an important strategy to minimize AMR. It comprises a set of interventions that aim to improve the use of antimicrobials, promoting the selection of the ideal drug regimen, consumption, dosage, duration of therapy and route of administration [9]. Multidisciplinary teams (physicians, pharmacists and nurses) are required to design, execute and monitor the actions of the ASP. The composition of the team may change depending on the structure and resources available in the organizations, but guidelines advocate the participation of the pharmacist in the ASP [1, 10]. In England, hospital clinical pharmacists are designated as promoters of evidence-based healthcare and cost-effective prescribing, and it is suggested that clinical pharmacy activities be improved for the proper management of anti-infective agents [11]. In addition, pharmacist-led ASPs have led to better patient outcomes, minimized AMR, and reduced healthcare costs [6].

In contrast, there are gaps and challenges in the consolidation of ASPs in hospitals where there were inadequate practices in relation to the use of antimicrobials or a lack of ASP-related activities [7]. Furthermore, the evaluation of the application of guidelines for the appropriate use of antimicrobials in ASPs is hampered by the lack of national protocols for the treatment of some infections [12]. In Brazil, there are also gaps in the role of pharmacists in the ASP and in the challenges that interfere with the consolidation of this program in hospitals [13, 14]. Therefore, this study aimed to assess the perspective of pharmacists on ASPs and the barriers to their consolidation in Brazilian hospitals.

Method

Type of study

This is a cross-sectional study. The STROBE checklist was used to report the results of the survey [15].

Population and sampling

According to data from the Federal Pharmacy Council (FPC), there were 234,301 pharmacists working in Brazil at the time the survey was planned [16]. Professionals who worked in day hospitals were excluded, as were those who worked exclusively in the outpatient sector or emergency care units due to the lower use of broad-spectrum systemic antimicrobials in these environments.

In order to ensure that the sample selected represented the population studied, a sample calculation was carried out to estimate the minimum number of participants according to Eq. 1 [17]:

$${\left(\frac{Z_{\alpha /2}\sqrt{p.q}}{E}\right)}^2$$ 1

Zα/2

critical value for the desired degree of confidence, usually: 1.96 (95%)

E

standard error, usually: ± 5% of the proportion of cases (absolute precision)

p

proportion of favorable results of the variable in the population

q

proportion of unfavorable results in the population (q = 1-p)

The calculation considered the number of pharmacists working in Brazil during the recruitment phase of the survey (September/2022), and the estimated number of pharmacists working in hospital pharmacies during this period (N = 6,771; 2.89%). A minimum sample of 43 pharmacists was therefore defined. The research was publicized, and the study population was invited to participate through the social media of the researchers and universities involved in the study. There was also support from organizations such as the FPC, Regional Pharmacy Councils and the Brazilian Society of Hospital Pharmacy.

Collection of data

The data were collected from December 2022 to January 2023 using an online self-completion tool developed and validated by the researchers. The validation process included content validity (to verify the adequacy of the items relative to the construct domains) and semantic validation (to verify comprehensibility by the study population) [18]. The data collected were on i) the profile of the pharmacists (gender, age, color, years of experience in antimicrobial stewardship (AMS), academic background, training in AMS); ii) the profile of the workplace (number of hospital beds, number of hospital ICU beds, ownership of the hospital, purpose or type of care provided by the hospital, location of the hospital (city and state), accreditation seal); iii) the pharmacists' confidence in carrying out their activities (confidence in participating in ASP meetings, recommending adjustments to antimicrobial doses, and recommending the use of antimicrobials in necessary or unnecessary situations); iv) perceived barriers to participation in the ASP (knowledge about antimicrobials, doctors’ views, communication with doctors and available ASP time); v) essential elements of the program (antimicrobial use protocol, sequential therapy protocol, electronic medical records and prescriptions, adequate financial resources, and adequate facilities); and vi) pharmacist participation in the program (participation in ward rounds, continuing education, meetings, audits and feedback, encouragement of sequential antimicrobial therapy, and counseling of doctors).

Statistical analyses

The data were tabulated in Microsoft Excel® 365 and analyzed using descriptive and analytical statistics. Quantitative variables were analyzed using measures of central tendency and dispersion compatible with their distribution profile; categorical variables were analyzed using absolute and relative frequencies. The Spearman ordinal correlation test was also used to assess correlations between variables, as well as the t-test and analysis of variance.

The data was analyzed using the Statistical Package for the Social Sciences, inc. (SPSS) Chicago, USA, version 26.0. The significance level used as a criterion for acceptance or rejection in the statistical tests was 5% (p < 0.05).

Results

Profile of the study participants

A total of 83 pharmacists took part in the study, the majority of whom were women (78.3%; n = 65), white (60.2%; n = 50), with an average age of 37 years (IQR = 11 years; Max = 56 years; Min = 25 years). More than half of the study participants had specializations (60.2%; n = 50) and there were professionals with master's degrees (27.7%; n = 23), doctorates (3.6%; n = 3) or just undergraduate degrees (8.4% n = 7). The majority of pharmacists worked in public hospitals (51.8%; n = 43), general hospitals (71.1%; n = 59) and hospitals that did not have an accreditation label (67.5%; n = 56).

Based on the responses obtained from study participants, the southeastern region of the country was that with the highest number of hospitals with ASPs implemented (Fig. 1). The states with the highest number of respondents were São Paulo (16.90%; n = 14), Minas Gerais (14.5%; n = 12), and Paraná (13.3%; n = 11).

Fig. 1.

Geographic distribution of pharmacists who presented data on perspectives and barriers in consolidating Antimicrobial Stewardship in Brazilian hospitals

It was also observed that 36.1% (n = 30) of the hospital pharmacists taking part in the survey had no experience in ASPs, although 53.3% (n = 16) of them had completed training or specialization courses involving ASPs, antibiotic therapy, the Hospital Infection Control Committee or related areas. It was also found that the professionals who had more experience in ASPs were the older ones (p = 0.038).

In addition, 45.8% (n = 38) of the respondents said they had an ASP in place in the hospital where they worked. Of these, 50% (n = 19) worked in public hospitals, 34.2% (n = 13) in private non-profit hospitals and 15.8% (n = 6) in private hospitals.

Public hospitals showed a greater tendency to have an ASP in place compared to the others, although there was no statistically significant difference (p = 0.952), with public hospitals (n_with ASP = 19; 23% versus n_without ASP = 24; 29%), private non-profit hospitals (n_{with ASP} = 13; 16% versus n_{without ASP} = 12; 14%) and private hospitals (n_{with ASP} = 6; 7% versus n_{without ASP} = 9; 11%). In hospitals with an ASP in place, pharmacists had a higher level of education (p = 0.025), more experience in ASPs (p = 0.019) and training in ASPs (p = 0.003).

According to the pharmacists, the consolidation of ASPs was more recurrent in accredited hospitals (n_{with ASP} = 17; 62.96% versus n_{without ASP} = 10; 37.04%) compared to non-accredited hospitals (n_{with ASP} = 21; 37.5% versus n_{without ASP} = 35; 62.5%). In addition, it was found that hospitals with an ASP had a greater number of beds in general (average with ASP = 233.2 beds; SD = 204.7 versus average without ASP = 228.2 beds; SD = 204.7; p = 0.006) and ICU beds (average with ASP = 34.8 beds; SD = 32.7 versus average without ASP = 30.1 beds; SD = 32.6; p = 0.026) compared to those without an ASP. The ASP strategies implemented in the hospitals are described in Table 1.

Table 1.

Report by pharmacists on the essential elements of the ASP used in Brazilian hospitals (n = 38)

Essential ASP Elements	n	N (%)
Clinical meetings	35	91.6%
ASP team members are aware of the importance of antimicrobial management	36	94.7%
Protocol for the use of antimicrobials	36	94.7%
Computerized medical records	35	94.6%
The hospital has electronic prescriptions	34	91.9%
Operational leadership of the program is an infectious disease specialist, clinical pharmacist or other professional with knowledge of infectious diseases	34	89.5%
Justification form for prescribing specific antimicrobials	31	81.6%
Process indicators for evaluating the consumption and use of antimicrobials	31	81.6%
Therapeutic monitoring of antimicrobials	26	72.2%
Adequate facilities for program development	24	63.2%
Antimicrobial audit and feedback	21	58.3%
Has access to computerized technologies for decision making	20	52.6%
Antimicrobial therapy descaling protocol	18	47.4%
Protocol for sequential antimicrobial therapy	17	45.9%
Adequate funding for the program	13	34.2%
Continuing education program on the use of antimicrobials	13	34.2%
System that allows automatic blocking of dispensing at the end of the proposed treatment	12	31.6%

Key: ASP: Antimicrobial Stewardship Program

Pharmacists with more experience in the ASP were more participative in encouraging sequential antimicrobial therapy (p = 0.014) and in decision-making at ASP committee meetings (p = 0.036). In addition, younger professionals in hospitals were more participative in evaluating antimicrobial consumption (p = 0.030) (Table 2).

Table 2.

Participation of pharmacists in the ASP of Brazilian hospitals by strategy (n = 38)

ASP Strategies	MP	Part	PP	NP	P-value
Monitoring the duration of antimicrobial therapy	51.4%	35.1%	13.5%	0.0%	0.000
Provision of an updated list of restricted-use antimicrobials available in the hospital to the medical team	28.9%	47.4%	21.1%	2.6%	0.001
Support for the maintenance of the electronic antimicrobial management program	31.6%	42.1%	18.4%	7.9%	0.017
Evaluation of antimicrobial consumption in the hospital	28.9%	42.1%	21.1%	7.9%	0.001
Development of protocols for the use/prescription of antimicrobials	28.9%	42.1%	21.1%	7.9%	0.025
Participation and decision-making at the ASP committee meetings	36.8%	31.6%	21.1%	10.5%	0.102
Implementation of the antimicrobial restriction policy	28.9%	36.8%	18.4%	15.8%	0.029
Stimulating Sequential Antimicrobial Therapy	26.3%	39.5%	26.3%	7.9%	0.053
Advising doctors on antimicrobial drug interactions	24.3%	35.1%	37.8%	2.7%	0.010
Medical advice on adverse reactions to antimicrobials	24.3%	34.2%	37.8%	2.7%	0.002
Audit and feedback on antimicrobial prescribing practices	18.4%	36.8%	26.3%	18.4%	0.324
Providing feedback to healthcare teams on the resistance profile of hospital-acquired infections	13.2%	34.2%	42.1%	10.5%	0.011

Key: MP: Very participative; Part: Participative; PP: Not very participative; NP: Not at all participative; ASP: Antimicrobial Stewardship Program

There was also greater confidence reported by pharmacists who had been trained in the following ASP strategies: recommendation of antimicrobial dosage adjustment based on pharmacokinetic and pharmacodynamic parameters (p = 0.006), recommendation of antimicrobial dose adjustment (p = 0.024), participation in discussions with AMS team (p = 0.012), recommendation of antimicrobial dose adjustment in relation to the type of bacteria (p = 0.008), recommendation of antimicrobial therapy or prophylaxis time adjustment (p = 0, 018), recommending the choice of antimicrobial to treat urinary tract infections (p = 0.038), recommending the choice of antimicrobial to treat community-acquired pneumonia (p = 0.038), and carrying out antimicrobial use audits to assess and report compliance with the antimicrobial restriction policy (p = 0.038) (Table 3). The confidence of pharmacists was higher in hospitals that have an ASP in place (average with ASP = 2.9; SD = 0.5329 versus average without ASP = 2.4; SD = 0.5270; p = 0.000).

Table 3.

Confidence of pharmacists participating in the study to work in ASP activities (n = 83)

Confidence of pharmacists	MC	C	PC	NC	P
Recommend adjusting the dose of antimicrobials	19.3%	53.0%	26.5%	1.2%	0.000
Recommend the choice of antimicrobial to treat urinary tract infections	10.8%	59.0%	27.7%	2.4%	0.000
Recommend the choice of antimicrobial to treat community-acquired pneumonia	10.8%	59.0%	27.7%	2.4%	0.000
Recommend adjusting the treatment time of antimicrobial therapy or prophylaxis	14.5%	51.8%	31.3%	2.4%	0.000
Recommend the choice of antimicrobial to treat hospital-acquired pneumonia	13.3%	51.8%	31.3%	3.6%	0.000
Recommend adjusting the dose of the antimicrobial considering the characteristics of the patient	15.8%	47.4%	32.9%	3.9%	0.000
Recommend antimicrobials in situations where their use is necessary	14.5%	47.0%	34.9%	3.6%	0.000
Conduct antimicrobial use audits to assess and report compliance with the antimicrobial restriction policy	16.9%	43.4%	32.5%	7.2%	0.000
Recommend not using antimicrobials in unnecessary situations	10.8%	44.6%	41.0%	3.6%	0.000
Participate in discussions with the ASP team	14.5%	39.8%	41.0%	4.8%	0.000
Recommend the choice of antimicrobial to treat skin and soft tissue infections	10.8%	42.2%	41.0%	2.4%	0.000
Recommend adjusting the antimicrobial dose according to the type of bacteria	11.7%	37.7%	48.1%	2.6%	0.000
Recommend the choice of antimicrobial to treat catheter-associated infections	8.4%	39.8%	44.6%	7.2%	0.000
Recommend the choice of antimicrobial to treat ventilator-associated pneumonia	12.0%	36.1%	41.0%	10.8%	0.000
Recommend empirical treatment with antimicrobials	12.0%	32.5%	45.80%	9.6%	0.000
Recommend adjusting the dose of the antimicrobial according to the site of infection	7.8%	36.4%	53.2%	2.6%	0.000
Recommend adjusting the dosage of antimicrobials based on pharmacokinetic-pharmacodynamic parameters	8.4%	28.9%	49.4%	13.3%	0.000

Key: MC: Very confident; C: Confident; PC: Not very confident; NC: Not at all confident; P-value: 5% (p < 0.05)

The barriers identified by the participants were significantly associated with being male. In this sub-group, the most cited barriers were: lack of access to reliable clinical and pharmacological information on antimicrobials in the hospital (p = 0.015) and support from their manager (p = 0.019). Similarly, there was a greater tendency for pharmacists with a higher level of professional training to report as a barrier the view of infectious disease doctors about their participation in the program (p = 0.040) and confidence about possible participation in the ASP (p = 0.043). In addition, support from the manager was more often reported as a barrier by pharmacists working in accredited hospitals (p = 0.032) (Table 4).

Table 4.

Barriers to the consolidation of ASPs in Brazilian hospitals from the perspective of pharmacists working in these establishments (n = 83)

Identified Barriers	Major impact	Some impact	Minor impact	No impact	p-value
Reduced number of pharmacists in the implementation of the ASP	60.2%	28.9%	9.6%	1.2%	0.000
Time spent on other pharmacy demands	48.2%	39.8%	9.6%	2.4%	0.000
Effectiveness of communication with doctors	45.8%	42.2%	12.0%	0.0%	0.000
Lack of access to safe clinical and pharmacological information on antimicrobials in the hospital	49.4%	37.3%	12.0%	1.2%	0.000
Confidence about their (possible) participation in the ASP	36.1%	42.2%	20.5%	1.2%	0.000
Discomfort in restricting antimicrobial access to patients when prescribed	25.3%	47.0%	27.7%	0.0%	0.000
Knowledge about antimicrobials (indications, dose, adverse effects, etc.)	37.3%	34.9%	27.7%	0.0%	0.000
Infectious diseases doctors' view	33.7%	34.9%	26.5%	4.8%	0.000
Importance given by doctors to the proper prescription of antibiotics and/or the policy of restricting these drugs	26.5%	41.0%	26.5%	6.0%	0.000
Support from your boss/supervisor	38.6%	28.9%	25.3%	7.2%	0.001
Time you have available during working hours	30.1%	37.3%	30.1%	2.4%	0.000
Support from the hospital administration	32.5%	26.5%	27.7%	13.3%	0.079

The correlation between confidence, barriers and the consolidation of ASP strategies in Brazilian hospitals from the perspective of pharmacists working in these establishments is presented in Fig. 2.

Fig. 2.

Correlation between confidence and barriers of ASP strategies in Brazilian hospitals from the perspective of pharmacists working in these establishments (n = 83). Key: ASP: Antimicrobial Stewardship Program

Also, according to the pharmacists, the situation of the hospitals in relation to the essential elements of the ASP revealed that adequate facilities for the operation of the program were more present in private hospitals (p = 0.023). Meanwhile, information technology resources were more present in specialized hospitals (p = 0.021). The justification form for prescribing specific antimicrobials was more prevalent in public hospitals (p = 0.031) (Table 5).

Table 5.

ASP strategies versus hospital characteristics

AMS Strategies	Type of Hospital			Expertise		Certification
	Pb	Pri	Par	G	E	Y	N
	(%)	(%)	(%)	(%)	(%)	(%)	(%)
Justification form for prescribing specific antimicrobials	54.8%	38.7%	6.5%	67.7%	32.3%	70.6%	29.4%
Protocol for the use of antimicrobials	52.8%	33.3%	13.9%	96.2%	30.6%	88.2%	11.8%
Sequential antimicrobial therapy protocol	52.9%	41.2%	5.9%	70.6%	29.4%	43.8%	56.3%
Antimicrobial therapy descaling protocol	38.9%	38.9%	22.2%	61.1%	38.9%	50.0%	50.0%
Therapeutic monitoring of antimicrobials	46.2%	34.6%	19.2%	65.4%	34.6%	70.6%	29.4%
Antimicrobial feedback audit	57.1%	38.1%	4.8%	66.7%	33.3%	47.1%	52.9%
Clinical meetings	45.5%	39.4%	15.2%	72.7%	27.3%	88.2%	11.8%
Continuous education program on the use of antimicrobials	46.2%	38.5%	15.4%	69.2%	30.8%	23.5%	76.5%
Process indicators for evaluating the consumption and use of antimicrobials	45.2%	38.7%	16.1%	67.7%	32.3%	82.4%	17.6%
Automatic blocking of dispensing at the end of the proposed treatment	50.0%	33.3%	16.7%	83.3%	16.7%	47.1%	52.9%

Key: Pb: Public; Pri: Private (non-profit—charitable or philanthropic); Par: Private (belonging to a legal entity governed by private law); G: General; E: Specialized; Y: Yes; N: No; ASP: Antimicrobial Stewardship Program; P-value: 5% (p < 0.05)

There was no statistical difference in the level of trust and barriers perceived by pharmacists in relation to the types of hospitals, the types of care and the presence of certification.

Discussion

The profile of the study participants showed that the majority of professionals were women, with an average age of 36 years (SD = 10.23) and a postgraduate degree (specialization, master's and/or doctorate), similar to the general profile of pharmacists in Brazil [19]. This attests to the qualitative representation of the study sample in relation to the profile of professionals working in the Brazilian pharmaceutical labor market. It is believed that the predominance of specialization in academic training is due to the wide range of lato sensu courses on offer and the limited supply of professional stricto sensu courses. In addition, the demand for specialization is generally associated with the search for skills for professional practice, while stricto sensu courses generally aim to train professionals to work in research and academia in general.

The reports of pharmacists showed that ASPs are present in less than half of hospitals in Brazil, which is similar to that obtained in a study involving all the states of the federation and evaluating hospitals with ICU beds [20]. In contrast, a study carried out in hospitals in the state of São Paulo showed that 85.0% of those interviewed reported having an ASP in place in the hospitals where they worked. It is believed that the difference in results regarding consolidation may have been influenced by the economic and technological development of this region of the country and that it could serve as a model for other regions [21].

Most of the participants were concentrated in the South and Southeast regions of Brazil, corroborating data from the National Health Confederation [22], which shows the centralization of hospitals in Brazil and the greater number of beds in these regions, known as the most developed in the country. This data also reflects the need to decentralize specialized hospitals to the Northeast, Midwest, and North regions of the country as a challenge for the health system [22].

The presence of an ASP was found to be predominant in public hospitals. In Australia, an ASP was present in 93.6% of public hospitals, while in France there was an ASP in 38.0% of public university hospitals and in 63.6% of general public hospitals. A different situation was found in Nigeria, where only 13.5% of hospitals had an ASP, all of which were teaching hospitals (21). In Brazil, it is believed that the predominance of ASPs in public hospitals can be explained by the 31% increase in the number of public hospitals and the 11% reduction in the number of private hospitals between 2010 and 2022 [22].

As in this study, a significant correlation was found between the presence of an ASP and a greater number of ICU beds [10]. This can be explained by the complex scenario of these environments, which generally contain patients with a critical general state of health, refractory to the action of broader-spectrum antimicrobials. In this context, the consolidation of the ASP becomes indispensable in order to optimize the selection of the antimicrobials needed for each patient and minimize the risk of AMR [13].

Regarding the participation of pharmacists in the ASP, the monitoring of antimicrobial consumption, dose adjustment and treatment duration were present in the studies as activities in which there was greater participation by pharmacists [10, 21]. French and Australian pharmacists reported greater self-confidence in carrying out activities such as recommending the adjustment of antimicrobial doses based on patients' clinical characteristics. In contrast, these professionals reported lower levels of confidence when recommending the adjustment of antimicrobials based on PK/PD (Pharmacokinetic-Pharmacodinamic) parameters. Participation in more complex ASP activities and the self-confidence to work in the program are linked to the completion of ASP courses. As an example, American pharmacists who are required to complete an American Society of Health pharmacy residency in infectious diseases in order to work in this area, are heavily involved in the most complex ASP activities in the hospitals where they work, optimizing doses and actively participating in the complex selection of antibiotics [10].

Regarding the perception of pharmacists in relation to the barriers to the consolidation of the ASP in Brazilian hospitals, the professionals who took part in the study cited factors such as the reduced number of pharmacists, the time allocated to other demands in the hospital pharmacy, the effectiveness of communication with doctors, and the lack of access to safe clinical and pharmacological information, similar to studies carried out in countries such as Australia and France [10]. The lack of time to carry out ASP activities, financial resources, support from doctors and the need for training in ASPs were also mentioned in surveys of French, Australian and Nigerian pharmacists, corroborating the data presented in this study. Thus, the results may reflect the lack of adequate resources to consolidate the ASP and reinforce the need for support, dedication of resources, and investment in education to ensure that pharmacists can work fully in the ASP [10, 21].

The differences in ASP activities implemented, participation, and barriers pointed out by pharmacists are also associated with variations in formal education and the provision of training in specific areas in each country [10]. For example, in Nigeria there is no formal education in infectious diseases, and only online ASP courses are available, but few pharmacists have taken them [21]. In contrast, in the United States, as mentioned, pharmacists who work in the management of infectious diseases need to have a postgraduate degree in this area. Similarly, in the UK, pharmacists have the opportunity to specialize in ASPs and infectious diseases when they work in the field. For Australian pharmacists, the opportunity to specialize in infectious diseases is not available, but in France there is a postgraduate course in antibiotic prescribing [10].

In light of this, studies agree that professional training and qualification in infectious diseases and ASPs, together with management support, are fundamental strategies for minimizing barriers [10, 21]. Therefore, postgraduate courses, residencies and online courses seem to be a viable strategy to increase the ability of pharmaceutical professionals to intervene and discuss assertively in this context. In addition, there is a need to include ASP strategies in the curriculum of undergraduate courses in order to start preparing these professionals for actions to prevent AMR in the professional sphere [21]. Furthermore, the need to qualify the training of pharmacists, especially for clinical work in the management of the use of antimicrobials, is also pressing, which is expected to be possible based on the recommendations expressed in the current National Curriculum Guidelines for Pharmacy Courses in Brazil, especially the competency-based training and the requirement that 50% of the workload should be in health care subjects [23].

The limitations of this study include the fact that online data collection may have discouraged pharmacists from participating in the survey. Although low participation rates have been identified in previous studies that also had online data collection, the choice of virtual environment and the collection strategy adopted allowed for economy, practicality, logistical feasibility, and proved to be adequate in the context of social isolation in which Brazil found itself during the data collection stage [24]. In addition, the use of technology through social media (Instagram®, Facebook®, Linkedin®) helped disseminate the research, and the organization of the database using Google Forms® facilitated data analysis.

The voluntary participation of the respondents may have generated a self-selection bias in the results. Furthermore, although the sample size was defined by mathematical calculations, the results may not reliably portray the Brazilian context. Not only is Brazil a country with a vast territory and notorious regional diversities, but it also has around 4,466 active hospitals, which considerably exceeds the number of hospitals characterized in this study based on the reports of the pharmacists who take part in the survey and work in them [22].

It is also believed that although the data collection tool was simple for respondents to fill in, its length and the time that pharmacists were supposed to spend filling it in may have deterred these professionals from taking part in the study. However, the tool was validated and it was found that it would be necessary to collect all the variables established in order to achieve the research objectives. In addition, the possibility of filling it out online made it easier for professionals to take part in the research, which could take place at any time that suited them best, unlike when the researcher is in person collecting data from the target population.

It is also important to highlight that as the unit of analysis in this study was the pharmacist and his/her perspectives on the ASP, regardless of which hospital this professional worked at, the frequency data generated quantitatively represent the point of view of the pharmacists participating in the research and not the distribution of AMS actions across Brazilian hospitals.

Finally, we recognize that this study offers a partial perspective on pharmacists' confidence in the ASP in the Brazilian healthcare system. Despite this, we believe that the results can be extended to other countries for a comprehensive understanding about the challenges and perspectives of implementing this program and the participation of pharmacists in this process. Additional research is needed to get a broader view of pharmacists' perception regarding their participation in an ASP in the Brazilian health system.

Conclusions

The ASP in Brazil, from the perspective of hospital pharmacists, was predominantly implemented in public hospitals, with a greater number of ICU beds and a greater number of beds in general. The main barriers to the development and consolidation of the ASP identified were related to local infrastructure, economic, and educational resources. The involvement of hospital and clinical pharmacists in implementing and consolidating AMS strategies in Brazilian hospitals has been shown to be associated with knowledge of AMS, training in AMS, and length of training. Therefore, actions are suggested to encourage and enable the participation of these professionals in the ASP, as well as promoting their qualification for this purpose.

Author contributions

The authors confirm contribution to the paper as follows: study conception and design: Carla Speroni Ceron, Jéssica Daniel Martins da Silva, Tiago Marques dos Reis; data collection: Carla Speroni Ceron, Jéssica Daniel Martins da Silva, Tiago Marques dos Reis; analysis and interpretation of results: Jéssica Daniel Martins da Silva, Lucas Borges Pereira, Fabiana Rossi Varallo, Mariana Martins Gonzaga do Nascimento, Larissa Helena Lobo Torres Pacheco, Paulo Roberto Maia, Carla Speroni Ceron e Tiago Marques dos Reis; draft manuscript preparation: Jéssica Daniel Martins da Silva, Lucas Borges Pereira, Fabiana Rossi Varallo, Mariana Martins Gonzaga do Nascimento, Larissa Helena Lobo Torres Pacheco, Paulo Roberto Maia, Carla Speroni Ceron e Tiago Marques dos Reis. All authors reviewed the results and approved the final version of the manuscript.

Funding

This study was financed in part by the Coordination for the Improvement of Higher Education Personnel – Brazil (CAPES) – Financial Code 001 and by the Federal University of Alfenas.

Declarations

Ethics approval

The study was approved by the Ethics Committee of the Federal University of Alfenas (UNIFAL-MG) under protocol number 5.239.322 and CAAE 52933621.2.0000.5142.

Conflict of interests

We have no conflicts of interest to disclose.