On March 12, 2020, the World Health Organization (WHO) declared a global pandemic of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), which is capable of causing coronavirus disease 2019 (COVID-19).1) The unprecedented advent and spread of this emerging infectious disease altered our social lifestyle by necessitating “social distancing” and brought about many challenges and changes to healthcare services.2,3) During the COVID-19 pandemic, healthcare services were offered to patients with COVID-19, the population at high risk for COVID-19, and the general population, and the need for healthcare services increased as a whole. Pharmacists, as healthcare workers, had the ability to respond to this crisis actively.
The U.S. Centers for Disease Control and Prevention recommended social distancing to prevent the spread of SARS-CoV-2 from person to person.4,5) However, social distancing campaigns placed limitations on maintaining a stable supply of healthcare services and mitigating the strain arising from the need for increased healthcare services, especially given the limited personnel and material resources available.6) Broadly, effective strategies, the identification of risk factors, and healthcare worker resource reallocation were required to respond to the increased social requirements of healthcare services.
Pharmaceutical care services include pharmacotherapy monitoring, patient counseling, and multidisciplinary team care for individual pharmacotherapy optimization and involve the pharmacist’s traditional role in preparing and distributing medication. 7) After the COVID-19 pandemic was declared, pharmacists implemented various pharmaceutical care services for COVID-19 prevention, diagnosis, and therapy, such as patient monitoring, clinical decision-making support, medication supply management, telemedicine, public health education, and personal protective equipment (PPE) supply management.8,9) Vaccination is an example of the extended legal authority of pharmacists’ role during the COVID-19 pandemic.10,11) The simulation model of a previous influenza A pandemic suggested that, when pharmacists participate in vaccination, the time required to immunize 80% of the adult population was reduced by 7 weeks.12) Pharmacists, as frontline healthcare workers, should take responsibility for applying practice by the classification of necessary pharmaceutical care services during the pandemic crisis.
This study aimed to review the implementation of pharmaceutical care services and to investigate further information on pharmaceutical care services for COVID-19 prevention, diagnosis, therapy, and vaccination during the COVID-19 pandemic by comprehensive review.
Four reviewers independently conducted this study and followed the Preferred Reporting Items for Systematic Reviews and Meta-analyses (PRISMA) 2020 guidelines.13) In this study, regular meetings with the reviewers were held to discuss and match opinions.
To identify acceptable articles, 3 databases (PubMed/Medline, Embase, and the Cochrane Library) were searched up to July 7, 2021. Keywords used during the search included “COVID-19,” “pandemic,” “coronavirus,” “pharmaceutical care,” “pharmacist,” etc. Eligible articles were limited to those published in English or Korean. Lists of references in previous review articles were also investigated for eligible studies. After excluding duplicate articles following the initial database search, the final eligible articles were determined by title, abstract, and full-text reviews.
All types of articles that reported the implementation of pharmaceutical care services by pharmacists during the COVID-19 pandemic were eligible for enrollment in this analysis. Duplicate articles, studies covering the implementation of pharmaceutical care services by other healthcare workers, non-COVID-19 articles, errata, papers on pharmacy education, articles not published in English or Korean, articles without available full-text versions, and veterinary articles were excluded from consideration.
The following data were extracted from included articles: article characteristics, details of the study design, characteristics of study targets, and items of pharmaceutical care services. Additionally, data extraction for each item of pharmaceutical care services was conducted via checking numbers “1” or “2” if articles reported that pharmacists implemented pharmaceutical care services or suggested that pharmaceutical care services should be implemented, respectively. Relevant characteristics of articles included the authors, received date (or date of online availability or conference presentation date), country, and type of article. The components of study design included the type of study design, study period, and practice setting (e.g., outpatients, including visitors to the community pharmacy; inpatients; facilities, and others). Study targets included patients with COVID-19, individuals at high risk of COVID-19, members of the general population, pharmacists, and healthcare workers other than pharmacists. Finally, pharmaceutical care services included the following:
Adverse drug reaction (ADR) monitoring, COVID-19 testing services, and medication therapy management (MTM)
Clinical decision-making support, clinical therapeutic drug monitoring (TDM), drug information (DI), healthcare worker education, interprofessional collaboration, and nutrition support team (NST) involvement
Electronic prescription (E-prescription) systems, home delivery services, medicine supply management, PPE management, medication refills, and vaccination
Patient consultations, psychological support, public health education, and telemedicine
Antibiotic stewardship programs (ASPs), clinical trial management, drug utilization evaluations (DUEs), pharmacotherapy guideline development, and policy development
“Medication therapy management” included in “patient evaluation and monitoring” indicates performing patient assessments, comprehensive medication reviews, and monitoring the efficacy and safety of medication therapy. “Clinical decision support” includes pharmaceutical care services that help healthcare professionals make treatment plans for patients. “Patient consultation and education” indicates pharmaceutical care services directly performed to the patient.
Extracted data were analyzed according to annual quarters to investigate changes in pharmaceutical care services over time. The primarily implemented pharmaceutical care services were determined according to setting, study target(s), the prevention of COVID-19, COVID-19 therapy, and vaccination. A meta-analysis and risk-of-bias assessment were not conducted, as descriptive articles were the most common article type included in this analysis. All analyses were performed using Microsoft Excel (Microsoft Corporation, Redmond, WA, USA).
On July 7, 2021, the 3 literature databases were searched using an adequate combination of keywords, yielding 3,564 articles. We excluded 638 duplicate articles as well as 206 non-COVID-19 articles, 1,303 articles that did not report on pharmaceutical care services delivered by pharmacists, 103 pharmacy education articles, 23 errata, and 72 articles not published in English or Korean. A full-text review of each remaining article (1,228 articles total) was performed, and the following were additionally excluded: 43 non-COVID-19 articles, 464 articles did not report on pharmaceutical care services delivered by pharmacists, 1 retracted article, 1 veterinary article, 29 pharmacy education articles, 8 previous review articles, and 8 articles without available full-text versions. Nine articles were further added by hand-searching the reference lists of previous review articles. Finally, 674 articles were included in this study (Supplementary eFig. 1).
Table 1 shows the characteristics of the articles included in this study. Studies from 100 countries reported on pharmaceutical care services, and 611 articles were reported from a single country. The time period most frequently reported on was the second quarter of 2020 (32.5%), followed by the third quarter of 2020 (21.2%) and the fourth quarter of 2020 (19.4%). Among the 674 included articles, more than half were descriptive studies (53.6%), while survey/interview studies were the second-most common type (17.5%). Studies conducted in the outpatient setting were most frequently reported (38.1%), followed by studies performed in an inpatient setting (25.1%). Individuals high risk for COVID-19 and patients with COVID-19 composed 67.8% of all study targets in this analysis. Fifty-four articles reported on the effects of the implementation of pharmaceutical care services. Supplementary eTable 1 shows a detailed list of medications used in studies for treatment or prevention of COVID-19.
We classified pharmaceutical care services into the 5 categories and 24 items, and counts of articles reporting on the implementation of different pharmaceutical care services by pharmacists are shown in Fig. 1. The most frequently reported pharmaceutical care service category was compounding/distribution/administration (n=465), followed by patient consultation and education (n=406). Separately, the most frequently reported pharmaceutical care service item was medicine supply management (n=184), followed by patient consultation (n=177).
Figure 2 shows counts of articles that reported on the implementation of pharmaceutical care services or suggested pharmaceutical care services that should be implemented, arranged quarterly. Most pharmaceutical care services were most frequently reported in the second quarter of 2020; in particular, medicine supply management was significantly covered at that time. Among those articles reporting data from the second quarter of 2020, medicine supply management was mentioned in 12.3%, followed by patient consultation (10.9%) and telemedicine (10.2%). Additionally, a suggestion was steadily offered that vaccination should be offered by pharmacists as a pharmaceutical care service from the first quarter of 2020 onward, but vaccination was only initiated by pharmacists starting in the first quarter of 2021.
In the analysis of pharmaceutical care services according to practice setting, medication refills, public health education, and home delivery services were covered by a high percentage of studies conducted in the outpatient setting, while ASP, DUE, and pharmacotherapy guideline development (in order) were covered by a high percentage of studies performed in the inpatient setting. In studies reporting on both out- and inpatient settings, policy development, healthcare worker education, and clinical TDM (in order) were frequently covered (Fig. 3a).
In the analysis according to study target, in studies of patients with COVID-19, clinical decision-making support and medicine supply management were mainly implemented (Fig. 3b). Telemedicine and patient consultation were commonly implemented for those reports on individuals at high risk for COVID-19. Studies of healthcare workers were mostly survey/interview studies and mainly reported on PPE management and patient consultation. Moreover, among 25 studies focusing on patients with severe COVID-19, clinical decision-making support (n=10) and medicine supply management (n=9) were frequently reported.
The reported rate of implemented pharmaceutical care services for COVID-19 prevention, diagnosis, therapy, and vaccination is represented in Fig. 3c. In studies investigating the prevention of COVID-19, public health education, PPE management, and medicine delivery services were mainly discussed, and COVID-19 testing services were mainly reported in studies on COVID-19 diagnosis. For therapy, the implemented pharmaceutical care services frequently reported included medication refills, DUE, clinical decision-making support, NST, and MTM, and vaccine administration was significantly covered in studies on COVID-19 vaccination. Additionally, in studies on COVID-19 treatment, the most-reported pharmaceutical care services were medicine supply management, clinical decision-making support, and MTM (Supplementary eFig. 2).
Among the articles reported in a single country, cumulative cases and cumulative deaths of COVID-19 that were reported by the WHO14) for each country to July 7, 2021, which was the database search date, and reported pharmaceutical care services are shown in supplementary eFig. 3. The United States, which had some of the highest cumulative case and cumulative death counts during the pandemic, reported many articles, and most pharmaceutical care services were implemented in its studies. Specifically, the top 5 ranking items of pharmaceutical care service implementation in the United States for COVID-19 were clinical decision-making support, telemedicine, MTM, medicine supply management, and patient consultation. The global COVID-19 mortality rate on July 7, 2021 was 0.022,14) with Peru, Egypt, and China experiencing >2 times the global COVID-19 mortality rate. Compared to the United States, China implemented most pharmaceutical care services. Egypt implemented the most pharmaceutical care services, except for medicine supply management, which was implemented as a top 5 pharmaceutical care services item in the United States. Only 1 article from Peru was included, and the implemented pharmaceutical care services were medicine supply management and clinical trial management.
Unprecedented infectious disease worldwide changes our social lifestyle. This study reviewed the pharmaceutical care services implemented by pharmacists for COVID-19 prevention, diagnosis, therapy, and vaccination through a systematic review. In this study, 24 pharmaceutical care services were classified into 5 categories, and the most frequently reported pharmaceutical care services item and category were medicine supply management and compounding/distribution/administration, respectively. Most of the enrolled articles reported data from the second quarter of 2020, and medicine supply management was significantly reported on during that time.
In the COVID-19 pandemic, the use of PPE, such as sanitizer and face masks, has been emphasized for the prevention of COVID-19,15,16) and an insufficiency of PPE supplies was a significant problem at that time.17) Australia and the United States reported a lack of medicine such as anesthetics, corticosteroids, cardiovascular drugs, and antibiotics because the supply of medicine was inadequate, and reports of inadequate stocks of medicine increased in these countries by 37 and 300%, respectively.18) Therefore, medicine supply management was also an important challenge to be overcome. In the included articles, to alleviate the lack of medicine and inappropriate distribution, medicine supply and PPE management were implemented as part of pharmaceutical care services. Furthermore, for continuing a sustained and stable supply and management of medicine and PPE, pharmacotherapy guidelines and policy development were implemented.
Following the first quarter of 2020, when the WHO declared the COVID-19 pandemic, the National Institutes of Health introduced the first management guideline for patients with COVID-19 on April 21, 2020.19) At the same time, the second quarter of 2020 was the time when articles most frequently reported on certain pharmaceutical care services, such as medicine supply management, patient consultation, telemedicine, clinical decision-making support, PPE management, and MTM.
The COVID-19 pandemic came 11 years after the H1N1 influenza pandemic in 2009. Although the H1N1 influenza pandemic emphasized and extended the function of pharmacists,20,21) the patterns and signs of infection by SARS-CoV-2 and H1N1 differ; therefore, the pharmaceutical care services were diversified. In particular, the implementation of “social distancing” to prevent infection transmission from person to person5) and the healthcare use patterns were altered for the COVID-19 pandemic. Patients with chronic diseases require continuous multidisciplinary management, and this correlated with healthcare problems among patients during the H1N1 influenza pandemic.21) During the COVID-19 pandemic, healthcare services and MTM to confirm the continuity of healthcare use were provided by telemedicine and home delivery services.
Healthcare workers’ burnout from an excessive workload was another medical problem seen during the COVID-19 pandemic.22,23) It is important that the distribution of human resources is efficient during a crisis of infectious disease. According to practice setting and targets, pharmacists should know which pharmaceutical care services should be preferentially implemented and adapted. The results of this study and the practice setting and targets of prior studies were associated. Studies on individual high risk for COVID-19 mainly took place in the outpatient setting, including community pharmacies (56.0%), and pharmaceutical care services that were implemented for the prevention of COVID-19 included telemedicine, patient consultation, home delivery services, and medication refill and E-prescription systems. In contrast, studies of patients with COVID-19 mostly took place in inpatient settings (69.2%), and the implemented pharmaceutical care services were pharmacotherapy guideline development, ASP, NST, clinical TDM, ADR, and clinical decision-making support. The patients that use healthcare services differ in accordance with the practice setting, and healthcare workers should be allocated considering the characteristics of both.
When pharmacists participate in vaccination programs, the rate of vaccination increases.24,25) The functions of pharmacists in vaccination campaigns increase the effect and safety of vaccines by way of patient education, checking of history and allergies, and ADR monitoring and by decreasing the workload of other healthcare workers. In this study, to prevent COVID-19, articles continuously suggested that the pharmacist should administer vaccines as a pharmaceutical care service from the first quarter of 2020 onward, but COVID-19 vaccination was only introduced as a pharmaceutical care service in the United States and United Kingdom from the first quarter of 2021 onward. Some countries reported barriers to the implementation of COVID-19 vaccination by pharmacists. To the best of this study’s knowledge, the United States, the United Kingdom, and Spain (specifically, Madrid) allowed pharmacists to administer the COVID-19 vaccine. Further studies need to confirm the effects of using pharmacists in the COVID-19 vaccination campaign, such as the rate of vaccination, changes in public perception, and adverse events of the COVID-19 vaccine.
Based on data from July 7, 2021, the United States, which had the majority of the number of reported articles, cumulative cases, and deaths from COVID-19, implemented the most pharmaceutical care services. China, Egypt, and Peru experienced >2 times the global COVID-19 mortality rate on July 7, 2021, and a simple comparison with the United States regarding the implementation of pharmaceutical care services could not be performed given variations in aspects such as the medical culture and insurance systems. However, it is meaningful to identify which pharmaceutical care services should be implemented first.
This is a meaningful study in that it provides an analysis of pharmaceutical care services during the COVID-19 pandemic according to the annual quarter, practice setting, and targets by systematic review. However, this study inevitably has several limitations. First, it did not include the latest article data. The situation of COVID-19 changes daily, and the guidelines or policies are evolving in response, so there are limitations to the collection of the latest data. Second, this study did not involve an analysis of pharmaceutical care services according to the total number of hospital beds. Instead, this study identified the most frequently implemented pharmaceutical care services by reporting the number of pharmacists per 1,000 people as reported in the Organisation for Economic Co-operation and Development and per the number of reported articles by countries. Finally, this study did not perform an analysis of correlations between cumulative cases and deaths from COVID-19 and the number of reported articles by countries. There are also confounders, such as differences in healthcare accessibility use and insurance systems. Further studies are needed to analyze these correlations.
For the prevention, diagnosis, therapy, and vaccination for COVID-19 in in- and outpatient settings, the implementation of pharmaceutical care services were identified by this study. If another infectious disease crisis arises, this study could support rearrangement of human resources and the implementation of pharmaceutical care services to prevent and treat such diseases.
During the COVID-19 pandemic, pharmaceutical care services are expanded globally. Moreover, pharmacists have participated in vaccination, clinical decision-making support, and telemedicine. Further studies are required to confirm the effects whether the participation of pharmacists on patients’ clinical outcomes during the pandemic.
This study was supported by the Korean College of Clinical Pharmacy Research Network Fund in 2021.
The authors have declared no potential conflicts of interest.