Shortages of “human medicinal products”, later referred to as “drug” shortages, are no longer a new phenomenon (Baumer et al., 2004; Fox et al., 2009; Pharmaceutical Group of the European Union, 2012; Collins, 2013; European Association of Hospital Pharmacists, 2014; De Weerdt et al., 2015a, 2017; Pauwels et al., 2015). Different wordings are used to describe drug supply problems and additional different interpretations are perceived when discussing drug shortages (De Weerdt et al., 2015b). In this paper, the wording “drug supply problem” is used, a term that covers “drug supply disruptions” (i.e., when the supply of drugs does not meet the demand at the level of pharmacies and wholesalers) and “drug shortages” (i.e., when the supply of drugs does not meet the demand at consumer/patient level).

Various causes of drug supply problems are described in literature (European Medicines Agency, 2012; Barlas, 2013; Birgli^®, 2013; Gupta and Huang, 2013; De Weerdt et al., 2015c). Reputational damage, economic and health implications, increased workload are just a few examples on how drug supply problems affect different stakeholders in the supply chain of delivering the medicinal products to patients (Fox et al., 2009; IMS, 2011; Kaakeh et al., 2011; Ventola, 2011; Havrilesky et al., 2012; Metzger et al., 2012; Pharmaceutical Group of the European Union, 2012; APB, 2015; De Weerdt et al., 2017).

Figure 1 displays a simplified supply chain for human medicinal products in Belgium. Two types of wholesalers exist in Belgium: (i) general wholesalers and (ii) full-line wholesalers. Full-line wholesalers, in contrast to general wholesalers, have several obligations and rights. For example, full-line wholesalers have the right to be supplied by the pharmaceutical companies. In turn, full-line wholesalers have the obligation to supply community pharmacies and to have a stock of two-third of all medicines available in Belgium (art 101) (Royal Decree Concerning Medicines for Humand and Veterinary Use, 2006).

In Belgium (including Flanders) hospital pharmacies order the majority of their products directly from the manufacturer. Only a small number of products available in hospital pharmacies are ordered by full-line wholesalers. Community pharmacies, on the other hand, must order their products via wholesalers (art 3) (Belgian Law on Medicines, 1964). Most frequently, a community pharmacy co-operates with one main full-line wholesaler and one back-up full-line wholesaler. In Belgium, a distinction is made between private and cooperative community pharmacies. Cooperative pharmacies engage for the purchase and distribution of medicinal products, resulting in mutual benefits for the pharmacies and patients. Due to the cooperation, pharmacies are able to exchange medicinal products between cooperative pharmacies within the same cooperation, which may be very beneficial for patients in case of short-term supply disruptions.

According to previous papers, European community pharmacies spend a lot of time on managing drug supply problems to avoid patients’ impact (Collins, 2013; APB, 2015; De Boer et al., 2015). At European level, a survey concludes that community pharmacists spend between 3 and 15 h a month on drug shortages (Pharmaceutical Group of the European Union, 2012; Medicine Shortages, 2016). Results of a previous questionnaire in the United Kingdom indicate a time spent of less than 1 h to more than 10 h per week on drug supply problems (Collins, 2013). However, it remains unclear which step in the management process consumes most time. Therefore, the aim of this study is to quantify the time employees of Flemish community pharmacies spend on drug supply problems as well as to investigate in detail which steps are most time consuming. In this way, sustainable measures can be formulated to mitigate the problem of drug supply problems.

A total of 35 community pharmacies started the study (about 1.33% of the Flemish community pharmacies), including 30 private community pharmacies and five cooperative community pharmacies. Eventually, 25 (i.e., 23 private and 2 cooperative community pharmacies) were retained for further analysis, which represents about 0.95% of the Flemish community pharmacies. Six community pharmacies dropped out and four community pharmacies were excluded based upon the exclusion criteria.

The starting sample (N = 35) and the final 25 pharmacies are representative to the Flemish situation in terms of the geographical distribution. Concerning the type of pharmacies, an underrepresentation is detected for cooperative community pharmacies. In 7 of the 25 community pharmacies included, only one pharmacist is employed. In 11 community pharmacies, the number of full time equivalent (FTE) pharmacists employed range from 1.25 to 2. Six pharmacies employ three FTE pharmacists and only one participating community pharmacy employ five FTE pharmacists.

Figure 2 represents the median time spent by the 25 community pharmacies, together with its IQR. The median time spent by the personnel of a community pharmacy on drug supply problems is 25 min per week, with a minimum of 14 min and a maximum of 38 min per week. The majority of the participating community pharmacists confirms our result, about six pharmacists argue that 25 min per week is too low. The minimum is observed in the week of Christmas (December 21, 2015) and community pharmacists attributed this minimum to more closing days during this period. The maximum of 38 min is observed in the second week of February. According to the participants, this can be explained due to an increase of ill persons or by certain drug shortages which required an increased time investment. This increased time investment is detected, among others, in an increase of communication with patients, informing them about the drug supply problem.

In Figure 2, several outliers are observed. These outliers represent great differences among the community pharmacies. As displayed in Figure 3, enormous differences in the reported times are observed among the 25 community pharmacies. The number of community pharmacies who spend on average less than 15 min per week practically equals the number of community pharmacies who spend more than 60 min per week on drug supply problems. About one-third of the community pharmacies spend on average between 15 and 30 min per week on drug supply problems.

Several aspects of a community pharmacy are considered as potential confounding factors, e.g., the number of patients helped per day, the number of prescriptions dispensed per day, the location of the community pharmacy and the stock management. However, no correlation is found between the total time spent by the community pharmacies and any of these factors (p > 0.5).

The most time consuming step is gathering information on drug supply problems, which corresponds to almost half of the total time spent by community pharmacists (Figure 4). This step includes checking the orders for missing products, contacting wholesalers and manufacturers and collecting more information on drug shortages via the website of the Federal Agency of Medicines and Health Products (FAMHP). The second most time consuming step is the communication toward patients and colleagues. Patients do not always understand why their product is in shortage and thus why they need to switch to a substitute. Ordering this substitute at another wholesaler or in case of quota at the manufacturer was the third most time consuming step.

Most of the time spent on managing drug supply problems is executed by the pharmacist himself (95%). The remaining 5% of the total time spent is accomplished by the pharmacy technician. It should be noticed that only 11 of the 25 community pharmacies have a pharmacy technician employed. Pharmacy technicians spend most of their time on contacting the wholesaler or manufacturer to receive more information on supply disruptions. Communication toward patients regarding the drug supply problems is the second most time consuming step for pharmacy technicians.

Flemish community pharmacies spend about 25 min on drug supply problems, with a minimum of 14 and a maximum of 38 min per week. The most time consuming step is searching for information on drug supply problems, which corresponds with almost half of the total time spent on managing drug supply problems.

The median time spent on drug supply problems by community pharmacies is much lower than previously reported (Pharmaceutical Group of the European Union, 2012; Collins, 2013). Previous research reveals a range on the time spent by United Kingdom community pharmacists going from less than 1 h a week to more than 10 h per week on managing drug shortages (Collins, 2013). However, of the 371 respondents, only 10% spend less than 1 h on drug shortages. Diverse explanations can clarify the observed difference with our result. First, differences in the applied research methodologies and semantics can result in differences in the time spent on drug shortages. A survey is often more subjective and therefore the result is probably an overestimation, while our study tries to be more objective. Second, national differences in the supply chain of community pharmacies might influence the time spent on drug supply problems.

In the United Kingdom, there are two main supply chains. The first one is similar to the Belgian supply chain (pharmaceutical industry to wholesalers and wholesalers to pharmacies). The second possibility to supply medicines in the United Kingdom is by pharmaceutical industry selling directly to pharmacies (DTP) and paying distributors or wholesalers a fixed fee for delivery (The Association of the British Pharmaceutical Industry [ABPI], 2017). Since the introduction of DTP-model, pharmacists spend apparently a lot more time on sourcing drugs, especially in comparison with the other “standard” supply chain (Kermani, 2010; The Pharmaceutical Journal, 2010). An important strength of the Belgian “standard” supply chain is that full-line wholesalers have medicinal products available of different pharmaceutical manufacturers. The DTP-model complicates the search toward generic or alternative medicines, which might result in an increased amount of time spent by community pharmacies in case of drug supply problems. However, more in-depth research is necessary to investigate the influence of the supply chain on the time spent by pharmacists on drug supply problems.

The time community pharmacists spend on drug supply problems (±25 min per week) also largely differs from the time spent by hospital pharmacists (±2 h per week) (De Weerdt et al., 2017). There are two important factors which can explain this difference: (i) the supply chain of pharmacies (see Figure 1) and (ii) the amount of products ordered. In Belgium, most hospital pharmacies order their products directly from the manufacturer and are mostly bound to tender-contracts. The size of the order in combination with limitations due to the contract complicates ordering the product with other manufacturers for hospital pharmacies. Community pharmacies, on the other hand, order their products from wholesalers. Smaller orders and the possibility of easily switching between full-line wholesalers for ordering generic or alternative medicines can clarify the observed difference between the time spent by hospital pharmacies and community pharmacies.

About 90% of the total time spent on drug supply problems is spent by the community pharmacist himself. Taken into account that seven community pharmacies employ only one pharmacist, a median time spent of 25 min per week on drug shortages, can be experienced as a real problem for such pharmacies. Especially since the time spent on drug supply problems is not delineated, but rather a constant reminder of the problem.

The study design has several advantages. By using self-reporting methodology, a relatively high number of community pharmacies could participate in the study (Emmerton and Jefferson, 1996; Rutter et al., 1998). Secondly, our results are based on the time spent by 25 private and cooperative community pharmacies. Thirdly, since drug supply problems vary over time, the widespread study period of 18 weeks is another advantage. However, on the other hand, this study period does not allow observing yearly fluctuations. A fourth bonus of this study consists of the profound way the issue of drug supply problems has been studied, which resulted in suggesting targeted measures (see further) to mitigate the problem.

This study provided exploratory results on the time spent by Flemish community pharmacists on drug supply problems as well as on the most time-consuming tasks within pharmacies. The sample of community pharmacies is relatively small, but representative for the Flemish situation and shows a large variation in the time spent. Though a median of 25 min per week seems not that much, the time spent on drug supply problems is not delineated and community pharmacists are constantly reminded of the problem. Further research in a larger sample of community pharmacies is needed to validate the results of this study. However, improving the provision of information about drug supply problems can reduce the total time spent by pharmacists. Similar results and recommendations were found for Belgian hospital pharmacies (De Weerdt et al., 2017).

All authors participated in the design of the study. ED performed data collection and analyzed the data and drafted the manuscript. IH, SS, and MC revised the manuscript critically and contributed to the interpretation of the data. All authors read and approved the final manuscript.

The work was financially supported by TEVA and the Research Foundation Flanders (FWO). The research was carried out independently by KU Leuven. None of the authors is employed by TEVA. MC is member of the Scientific Advice Working Party at EMA. The other authors declares that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.