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Article

11-Year Trend in Antibiotic Consumption in a South-Eastern European Country; the Situation in Albania and the Implications for the Future

by
Iris Hoxha
1,*,
Brian Godman
2,3,*,
Admir Malaj
4 and
Johanna C. Meyer
3,5
1
Department of Pharmacy, Faculty of Medicine, University of Medicine Tirana, 1001 Tirana, Albania
2
Department of Pharmacoepidemiology, Strathclyde Institute of Pharmacy and Biomedical Sciences, University of Strathclyde, Glasgow G4 0RE, UK
3
Department of Public Health Pharmacy and Management, School of Pharmacy, Sefako Makgatho Health Sciences University, Ga-Rankuwa 0208, South Africa
4
Independent Researcher, 1001 Tirana, Albania
5
South African Vaccination and Immunisation Centre, Sefako Makgatho Health Sciences University, Molotlegi Street, Garankuwa, Pretoria 0208, South Africa
*
Authors to whom correspondence should be addressed.
Antibiotics 2023, 12(5), 882; https://doi.org/10.3390/antibiotics12050882
Submission received: 31 March 2023 / Revised: 2 May 2023 / Accepted: 6 May 2023 / Published: 9 May 2023
(This article belongs to the Special Issue Antibiotics Use in Infection and Public Health)
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Abstract

:
There are growing concerns with rising antimicrobial resistance (AMR) across countries. These concerns are enhanced by the increasing and inappropriate utilization of ‘Watch’ antibiotics with their greater resistance potential, AMR is further exacerbated by the increasing use of antibiotics to treat patients with COVID-19 despite little evidence of bacterial infections. Currently, little is known about antibiotic utilization patterns in Albania in recent years, including the pandemic years, the influence of an ageing population, as well as increasing GDP and greater healthcare governance. Consequently, total utilization patterns in the country were tracked from 2011 to 2021 alongside key indicators. Key indicators included total utilization as well as changes in the use of ‘Watch’ antibiotics. Antibiotic consumption fell from 27.4 DIDs (defined daily doses per 1000 inhabitants per day) in 2011 to 18.8 DIDs in 2019, which was assisted by an ageing population and improved infrastructures. However, there was an appreciable increase in the use of ‘Watch’ antibiotics during the study period. Their utilization rose from 10% of the total utilization among the top 10 most utilized antibiotics (DID basis) in 2011 to 70% by 2019. Antibiotic utilization subsequently rose after the pandemic to 25.1 DIDs in 2021, reversing previous downward trends. Alongside this, there was increasing use of ‘Watch’ antibiotics, which accounted for 82% (DID basis) of the top 10 antibiotics in 2021. In conclusion, educational activities and antimicrobial stewardship programs are urgently needed in Albania to reduce inappropriate utilization, including ‘Watch’ antibiotics, and hence AMR.

1. Introduction

There are concerns with rising rates of antimicrobial resistance (AMR) globally, increasing morbidity, mortality, and costs [1,2,3,4,5,6]. In 2019, there were an estimated 1.27 million deaths globally directly attributable to AMR with 4.95 million associated with bacterial AMR and rising [7]. As a result of this alarming trend, AMR is now often seen as the next pandemic [8]. Multiple international, regional, and national activities have been instigated in recent years to reduce AMR. These include the instigation of the World Health Organization (WHO) Global Action Plan to reduce AMR, translated into National Action Plans (NAPs) across a number of countries and continents [1,9,10,11,12,13]. Other key activities driven by the WHO include the instigation of the AWaRe classification, which divides antibiotics into ‘Access’, ‘Watch’, and ‘Reserve’ groups depending on their resistance potential, with greater resistance potential for antibiotics included in the ‘Watch’ and ‘Reserve’ groups, as well as more recently, prescribing guidance [14,15,16]. The initial target to reduce AMR is that at least 60% of antibiotic utilization within a sector or country should be ‘Access’ antibiotics, with ‘Watch’ and ‘Reserve’ antibiotics limited in their utilization [17,18,19]. This is a key issue among low- and middle-income countries (LMICs), with their increasing utilization of ‘Watch’ antibiotics driving up AMR [18,19].
We have seen a number of Central and Eastern European (CEE) countries, as well as former Soviet Union Republics, which are not included in CEE countries, introduce or plan to introduce a number of initiatives and activities to reduce inappropriate utilization of antibiotics and ultimately AMR [20,21,22,23,24,25,26]. In Armenia, total antibiotic consumption decreased from 15.9 defined daily doses (DDDs) per 1000 inhabitants per day (DIDs) in 2011 to 10.7 DIDs in 2015 through targeted awareness campaigns and other initiatives by a multi-sectorial group at the Ministry of Health [23]. In Slovenia, multiple activities, which included prescribing restrictions via the Ministry of Health and the Health Insurance Agency, resulted in a 31% decrease in antibiotic consumption between 1999 and 2012 [20]. Such activities and dynamics contrast with the documentation of increased consumption of antibiotics in Serbia in recent years. Antibiotic utilization rose from 26.4 DIDs in 2011 to 36.5 DIDs in 2015 with limited demand-side measures introduced by the Government of Health Insurance Agency to influence physician prescribing [23]. Similarly in Poland, a lack of demand-side measures among key stakeholder groups helped to maintain continued high antibiotic utilization rates [27]. This included appreciable prescribing of broad-spectrum antibiotics, thereby enhancing resistance rates [27]. Overall, cultural and other factors, including resistance to change alongside regulations, play a key role in addition to other governance factors, with influencing antibiotic prescribing and dispensing patterns [28,29,30,31,32,33]. This includes issues of corruption surrounding governance in healthcare across Europe with poor governance increasing inappropriate antibiotic use and hence AMR [34,35].
Albania is an upper middle-income country in South-East Europe with a population of just under three million in recent years [36]. However, the population in Albania is ageing, which will impact on future medicine use as well as the adequacy of healthcare funding. Good governance in a country is important to tackle AMR [34]. This is a concern in Albania, with Albania currently ranked 101 out of 180 countries in terms of perceptions of corruption [37]. There are also concerns regarding current knowledge of key stakeholder groups in Albania regarding antibiotics and AMR [38,39]. Alongside this, there are concerns regarding the current lack of antimicrobial stewardship (AMS) activities in Albania to influence future utilization. In addition, despite current legislation prohibiting the purchasing of antibiotics without a prescription, this still occurs, exacerbated by patient pressure and weak governance [34,38,40,41,42]. We have seen in other ex-communist countries that increased knowledge among pharmacists, coupled with guidelines and greater monitoring of the legislation, has appreciably reduced the purchasing of antibiotics without a prescription, providing guidance to key groups in Albania [43]. There are also concerns with current antibiotic prescribing patterns in hospitals in Albania. This includes their prolonged use post-operatively to prevent surgical site infections (SSIs) [44]. Previous published studies have also documented appreciable utilization of ‘Watch’ antibiotics in Albania compared with other European countries [45,46]. This is also a concern as high inappropriate use of ‘Watch’ antibiotics will drive up AMR [18,19].
Consequently, in view of ongoing concerns in Albania, we believe there is a need to build on previous publications that have tracked antibiotic utilization patterns in Albania, including high rates of ‘Watch’ antibiotics. [23,45,46]. This is important with delays in the approval of the Albanian NAP to reduce AMR, which was drafted in October 2017 [47]. The tracking of antibiotic utilization patterns can be used as a starting point for examining and debating future strategies to address utilization patterns of concern, such as excessive use of ‘Watch’ antibiotics, as seen in Estonia and Slovakia [24,26]. Alongside this, we examine whether issues, such as perceived levels of corruption or changes in the wealth of a country in terms of gross domestic product (GDP), as seen in Albania, appear to influence antibiotic use. Such findings can also form part of future strategies to reduce AMR in a country. Our findings, alongside exemplars from other European countries and beyond, can subsequently be used to suggest additional strategies that could be undertaken by key stakeholder groups in Albania to improve future antibiotic utilization patterns and reduce AMR if concerns still exist. Currently, no additional activities appear to have been undertaken in Albania in recent years to improve future appropriate antimicrobial utilization among patients in line with the goals of the NAP. This also needs to be addressed.
Alongside this, we are aware that there has been an appreciable increase in the use of antibiotics in patients with COVID-19 across countries and sectors despite limited evidence of bacterial infections or co-infections [48,49,50,51,52,53], which might represent significant levels of inappropriate use. Consequently, there is also a need to examine antibiotic utilization trends during the pandemic in Albania alongside the implications.
In view of this, the objectives of this study were to measure and analyze antibiotic utilization patterns in Albania in recent years alongside possible factors influencing these patterns. Potential factors include an ageing population, increasing GDP, as well as current levels of corruption. The findings, along with exemplars from other countries, can subsequently be used to give guidance to key stakeholder groups in Albania and beyond.

2. Results

We will first discuss the broader antibiotic utilization patterns in Albania during the past 11 years using a traditional drug utilization approach before looking critically at their composition, including trends in the utilization of ‘Watch’ antibiotics. In addition, we assess the possible impact of key factors, including an ageing population and governance, on utilization patterns. There is no attempt to look critically at the utilization of individual antibiotics because there is no diagnostic or indication data in the data sets used for analysis. In addition, the lack of specific demand-side measures at set times precludes the use of sophisticated statistical analyses, including time series analyses.

2.1. Utilization Patterns

Total antibiotic consumption fell in Albania between 2011 and 2019 but increased thereafter until 2021, which coincided with the COVID-19 pandemic (Figure 1). There was a similar pattern in the overall utilization of the top 10 antibiotics. Their percentage utilization accounted for 69% to 81% of total antibiotic utilization during the study period. However, there was no obvious overall prescribing pattern during this period in terms of their percentage of total utilization. This is different to the utilization pattern of ‘Watch’ antibiotics. Their utilization appreciably increased from 10% of total utilization among the top 10 most utilized antibiotics (DID based) in 2011 to 82% in 2021. This is further illustrated in Figure 1 and Figure 2.
Overall, in 2011 only two antibiotics from the ‘Watch’ list were present in the list of the top 10 most utilized antibiotics in 2011. This had appreciably changed by 2021 when only two of the antibiotics in the top 10 were from the ‘Access’ list; the remainder were from the ‘Watch’ list (Table 1). Table 1 documents the increasing utilization of azithromycin as well as levofloxacin and other ‘Watch’ antibiotics during the study period.

2.2. Potential Influencing Factors

Table 2 shows potential factors that could have contributed to increased or decreased antibiotic utilization in Albania between 2011 and 2021.
Table 3 shows the Kendall’s tau-b correlation coefficients between antibiotic use and other potential factors. A strong correlation between the median age of the population and antibiotic utilization until the start of the pandemic (2011–2020) was observed. This may reflect reduced requests for antibiotics to treat children with acute respiratory diseases during this period with ageing populations. Between 2011 and 2020, there was a significant correlation with GDP per capita, while no correlation was observed with the corruption index (Table 3).
There is a significant correlation between the decrease in antibiotic use and an increase in median age for the period 2011–2020. A similar significant correlation is observed between the decrease in antibiotic use and the growth in GDP per capita. It must be noted that these correlations are significant only when the 2021 values, which we considered outliers, are excluded (Table 3).
The scatter plots in Figure 3 illustrate a potential relationship between antibiotic consumption and median age of the Albanian population and GDP per capita, with the value for year 2021 considered an outlier. We do not see any potential relationship between antibiotic consumption and the corruption index score.

3. Discussion

We believe this is the first study undertaken in Albania in recent years to document current antibiotic consumption through an 11-year study as well as changes in utilization patterns prior to the introduction of the NAP. This includes changes in patterns following the recent COVID-19 pandemic. Prior to the pandemic, we saw a decreasing trend in the overall utilization of antibiotics in Albania from 27.2 DIDs in 2011 to 18.8 DIDs in 2019. We believe this is primarily due to ageing populations with less childhood respiratory illnesses. Such a correlation is supported by the fact that over 90% of antibiotic utilization globally is in ambulatory care, with only a minority in hospital care, especially in LMICs [16,55]. Alongside this, ageing populations will mean less prescribing of antibiotics for self-limiting upper respiratory tract infections (URTIs) in children, with URTIs currently accounting for an appreciable proportion of antibiotic utilization in ambulatory care in LMICs [16,56]. In addition, strengthening of the healthcare system coupled with improved living standards, alongside improved community infrastructures (Table 3), may also have contributed to less transmission of communicable diseases and consequently lower utilization of antibiotics [34,57]. This is because we are unaware of systematic educational and other activities in Albania in recent years to address concerns with variable knowledge of key healthcare professionals (HCPs) regarding antibiotics and AMR and the subsequent impact on patient and physician behavior [38,42]. The high empiric use of antibiotics in these studies reflects a lack of culture and sensitivity testing, which coupled with patient pressures on physicians and pharmacists to prescribe and dispense antibiotics [38,42], needs to be addressed to reduce AMR in the future.
These pressures, coupled with increasing concerns with AMR, may have also contributed to the increasing use of ‘Watch’ antibiotics in recent years. In 2011, only two antibiotics from the ‘Watch’ list were in the top 10 most utilized antibiotics in Albania (Table 1, Figure 2). However, by 2019, antibiotics in the ‘Watch’ list accounted for seven of the top ten antibiotics and 70% of total usage of the top ten antibiotics. This is appreciably higher than the 60% target for ‘Access’ antibiotics within total antibiotic utilization in countries established by the WHO [16,17,19,55]. We are unable to comment further on this, alongside any statistical analysis, without additional studies and more sophisticated datasets. In any event, this trend needs to be urgently addressed to reduce AMR rates in Albania.
It is difficult to also comment on trends in the utilization of antibiotics in hospitals in Albania during the study years, including IV versus oral use, as we were unable to disaggregate the utilization data into separate sectors and components. However, there have been concerns in previous studies with prolonged antibiotic administration post-surgery to reduce SSIs in Albania [44]. This may be driven by concerns with coverage and resistance rates, with the potential for greater prescribing of ‘Watch’ antibiotics if there is high empiric prescribing with currently limited culture and sensitivity testing in hospitals in Albania, which is similar to a number of other countries documented in recent studies and reviews among LMICs [58,59]. Again, we are unable to comment further without additional research. However, we are aware that antimicrobial stewardship programs (ASPs) have been successfully introduced in a number of LMICs to reduce prolonged prescribing of antibiotics post-operatively to prevent SSIs (Table S1—Supplementary Materials). This is welcomed as there have been concerns with the instigation of ASPs among LMICs due to resource issues both in terms of personnel as well as the necessary financial resources needed for their instigation [60]. The implementation of ASPs can also help rapidly progress patients from IV to oral equivalents to hasten discharge where pertinent [61,62]. This is because we have seen the number of IV packs purchased increasing in Albania in recent years, especially in particular during the pandemic years (I Hoxha personal communication). These various ASP studies can act as exemplars to key stakeholder groups involved with hospital prescribing of antibiotics in Albania going forward as they start to implement the NAP.
Another identified concern is the increased utilization of antibiotics following the COVID-19 pandemic, which reversed the downward utilization trend that was seen (Figure 1). Such an upward trend seemed to have overridden previous influencing factors, including ageing populations, GDP, and corruption. The reasons for this trend are uncertain. However, this may demonstrate the considerable focus on managing patients with COVID-19 in Albania since the start of the pandemic, with this trend matching the increasing use of antibiotics seen in other countries during the pandemic [48,50,51]. This trend is difficult to justify as there is little evidence of bacterial infections in these patients [51,63,64]. This signals appreciable inappropriate prescribing in Albania, which again urgently needs to be addressed.
The increasing use of ‘Watch’ antibiotics, now accounting for 82% of total antibiotic utilization among the top 10 most utilized antibiotics during the pandemic, is also a considerable concern. This excessive use may have been driven by physicians feeling more comfortable with prescribing ‘Watch’ antibiotics to feel safer in the absence of resistance data with limited testing in reality. However, again, we cannot comment further without additional research. In any event, this trend also needs to be urgently reversed. Table S2 in the Supplementary Materials provides examples of ASPs that have been successfully undertaken in LMICs to improve physician prescribing of antibiotics. These examples are again welcomed given earlier concerns with successfully instigating ASPs in LMICs [60], providing exemplars to key stakeholder groups in Albania at this critical time as they start to again implement their NAP. Table S2 also provides examples of successful programs introduced in LMICs to reduce the purchasing of antibiotics without a prescription, which has also been documented as a concern in Albania despite current legislation [38,41].
We are also likely to see a greater use of prescribing indicators across countries, including Albania, centered on the AWaRe book with their treatment suggestions for a number of infections routinely seen across sectors [16,55]. This is seen as a key way of reducing AMR [16,17,55]. Other key activities that could be undertaken in Albania to improve the use of antibiotics include improving the education of all healthcare students, especially physicians and pharmacists, regarding their appropriate use. The curriculum should include current guidelines and their rationale, such as the AWaRe book, alongside input into AMR and ASPs. Making sure physicians and pharmacists are aware of the likely origins of infections, such as URTIs and COVID-19, and the limited impact on patient care with antibiotics, should also be part of the curricula as well as the likely impact of their overuse, including adverse reactions and AMR. Educational input should also be provided post qualification through lifelong mandatory education. This is because we have seen educated pharmacists in LMICs be proactive with the use of guidelines to reduce unnecessary dispensing of antibiotics without a prescription, which includes patients with COVID-19, and this can be applied in Albania (Table S2) [43,65,66,67]. These campaigns have worked in other LMICs providing direction to key stakeholders in Albania as they seek to implement the NAP as well campaigns among patients regarding antibiotics, viral infections, and AMR to reduce their requests for antibiotics among both physicians and community pharmacists [56]. This will be a growing area among LMICs, with most studies to date on patient education conducted among higher-income countries [56]. We will be following this up in future research projects building on this study for which the strength is a long follow-up period using standard drug utilization methodologies endorsed by the WHO [23,45,68,69]. Overall, to enhance the appropriate use of antibiotics in Albania, the MoH in Albania will need to firstly reinforce the monitoring of the prescribing and utilization of antibiotics across sectors as well as within the distribution chain as part of NAP activities. Secondly, the various institutions need to foster education and awareness regarding antibiotics, AMR, and ASPs with all HCP groups as well as with the patient population at large. Thirdly, the various institutions and the MoH need to provide the necessary equipment and tools to HCPs to increase prescription accuracy and protocol compliance in line with AWaRe guidance.
We are aware of a number of limitations with this study. These include the fact that we could not split the utilization data down into ambulatory and hospital sectors for comparison purposes. In addition, since the data were aggregated, we were unable to break this down into the different formulations. There were also no diagnostic or resistance data to assess the appropriateness of prescribing, especially the ‘Watch’ antibiotics. Alongside this, data sets post pandemic were limited to undertake sophisticated statistical analysis of any trends. Despite these limitations, we believe our findings are robust based on the length of this longitudinal study and breaking antibiotic utilization patterns down into the different AWaRe components. Alongside this, potential different hypothesis and factors should be tested to guide all key stakeholders in Albania going forward when the NAP will be launched.

4. Materials and Methods

Antibiotic utilization patterns for the total population of Albania from 2011 to 2021 are documented as DIDs (defined daily doses per 1000 inhabitants per day). DIDs are an internationally recognized metric used by the WHO for undertaking drug utilization studies to meaningfully document drug utilization patterns across countries, including European countries, where there are appreciable differences in population sizes [23,26,45,69]. Individual antibiotics are broken down by their anatomical therapeutic chemical (ATC) and AWaRe classifications for comparative purposes as well as providing targets for future ASPs [14,15,70]. The ATC/DDD index toolkit from 2011 to 2021 was used for each respective year to calculate consumption for comparative purposes. The ATC and DDD methodologies are internationally recognized for analyzing utilization trends both within and across countries [20,68,69,71,72].
The AWaRe classification is important given previously high rates of ‘Watch’ antibiotics being prescribed and dispensed in Albania [23]. In this system, the ‘Access’ group are typically considered as first- or second-line antibiotics for up to 26 common or severe infections, generally with a narrow spectrum and low resistance potential. The ‘Watch’ group have a higher resistance potential and greater side effects, with the ‘Reserve’ group only recommended as last resort for severe infections [14,15,17,55].
We also listed the number of antibiotics in the ‘Watch’ vs. ‘Access’ categories each year in the top 10 most utilized antibiotics since these are the most prescribed. We chose the top 10 as this usually encompasses most of the utilized antibiotics and gives a good focus for future ASPs. Examples of successful ASPs will also be documented to give guidance to all key stakeholder groups across the sectors in Albania to improve future antibiotic prescribing and dispensing where concerns have been identified. This though will not be a systematic review of successful examples in the three key situations, e.g., hospital antibiotic prescribing to prevent SSIs, initiatives to improve physician prescribing, as well as initiatives to appreciably reduce the purchasing of antibiotics without a prescription. This is because one of the primary objectives of this paper is to provide examples to key stakeholder groups in Albania regarding successful approaches that have been implemented in other LMICs to address concerns with utilization patterns where these are seen rather than undertake full systematic reviews. These examples from the literature are based on the considerable experiences of the co-authors publishing in this area [10,20,21,43,56,58,73]. These examples can subsequently be appraised by key stakeholder groups in Albania for their local suitability as the government and others in Albania seek to reduce AMR in line with the goals of the NAP. This builds on similar situations that some of the co-authors have been involved with across LMICs [10,56,58,73]. We concentrated on ASPs and their impact rather than any cost-effectiveness analyses of possible different interventions as we are aware that most of these have been undertaken in high income countries [74,75,76,77]. Consequently, the approaches may not be totally suitable for LMICs [60].
The source of the antibiotic utilization data was the import records provided from the Drug Agency and Customs in Albania combined with the sales records from local manufacturers. This encompasses the total population of Albania.
EUROSTAT with INSTAT (Albanian Institute for Statistics) provided population data [36], with the World Bank and Transparency International providing data on GDP as well as the corruption index [37,54]. GDP data is important, especially in countries with high co-payment levels for medicines as well as those where there is appreciable purchasing of antibiotics without a prescription as seen in Albania [38,41]. The corruption index is also important where regulations need to be enforced to reduce the inappropriate use of antibiotics, including their dispensing without a prescription [32,33]. The age profile of patients is also important with, as mentioned, over 90% of antibiotic utilization across countries, typically in ambulatory care coupled with considerable over prescribing and dispensing of antibiotics for essentially viral infections, including coughs and colds, among children [16,17,56,73].
The Kendall’s tau-b correlation coefficient with 95% confidence interval (two-tailed) was calculated to test potential associations between antibiotic utilization patterns and potential key factors using IBM SPSS Statistics (version 26). Two-sided p-values < 0.05 were considered statistically significant. Scatterplots were subsequently created using Microsoft Excel to illustrate potential associations.
There was no ethical approval for this study as no patients were involved. In addition, data was extracted from publicly available datasets. This is in line with institutional guidance.

5. Conclusions

In conclusion, there are principally three challenges to address in Albania to improve future antibiotic use given current concerns, especially with the growing use of ‘Watch’ antibiotics. Firstly, key stakeholders need to reinforce and implement the draft NAP leveraging multi-sectorial. Secondly, ASPs need to be urgently introduced in hospitals to address concerns with excessive prescribing of antibiotics. This includes any prolonged use to prevent SSIs, any prolonged IV administration, or excessive prescribing in patients with COVID-19. Thirdly, universities need to make sure in their curricula that all key HCP students are fully conversant with the rationale for prescribing antibiotics, especially ‘Watch’ antibiotics’, as well as undertaking ASPs post-graduation.
Lastly, the MoH in Albania will need to reinforce the routine monitoring of prescribing and utilization of antibiotics across sectors as well as provide the necessary equipment and tools to HCPs to increase prescription accuracy and protocol compliance in line with AWaRe guidance.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/antibiotics12050882/s1, Table S1: Programs instigated among a selection of LMICs to improve antibiotic prescribing for surgical antibiotic prophylaxis (SAP) patients; Table S2: Initiatives to improve antibiotic utilization among physicians and pharmacists in ambulatory care in LMICs. References [78,79,80,81,82,83,84,85,86,87,88,89,90,91,92,93,94,95,96,97,98,99,100,101,102,103,104,105,106,107,108,109,110,111,112,113] were cited in the Supplementary Materials file.

Author Contributions

Conceptualization and methodology: I.H., A.M., J.C.M. and B.G.; investigation, analysis, and validation: I.H. and A.M.; interpretation: I.H., A.M., J.C.M. and B.G.; writing original draft: I.H. and B.G.; further drafts: I.H., A.M., J.C.M. and B.G.; administration: I.H. and B.G. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

There was no ethical approval for this study as no patients were involved. In addition, data were extracted from publicly available datasets. This is in line with institutional guidance.

Informed Consent Statement

This was not necessary as no patients were involved in this research.

Data Availability Statement

Additional data are available on reasonable request from the co-authors. However, all sources have been referenced.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. World Bank Group. Pulling Together to Beat Superbugs Knowledge and Implementation Gaps in Addressing Antimicrobial Resistance. 2019. Available online: https://openknowledge.worldbank.org/bitstream/handle/10986/32552/Pulling-Together-to-Beat-Superbugs-Knowledge-and-Implementation-Gaps-in-Addressing-Antimicrobial-Resistance.pdf?sequence=1&isAllowed=y (accessed on 28 April 2023).
  2. OECD Health Policy Studies. Stemming the Superbug Tide. 2018. Available online: https://www.oecd-ilibrary.org/sites/9789264307599-en/index.html?itemId=/content/publication/9789264307599-en&mimeType=text/html (accessed on 26 April 2023).
  3. O’Neill, J. Tackling Drug-Resistant Infections Globally: Final Report and Recommendations—The Review on Antimicrobial Resistance. 2016. Available online: https://amr-review.org/sites/default/files/160525_Final%20paper_with%20cover.pdf (accessed on 26 April 2023).
  4. Hofer, U. The cost of antimicrobial resistance. Nat. Rev. Microbiol. 2019, 17, 3. [Google Scholar] [CrossRef]
  5. Cassini, A.; Högberg, L.D.; Plachouras, D.; Quattrocchi, A.; Hoxha, A.; Simonsen, G.S.; Colomb-Cotinat, M.; Kretzschmar, M.E.; Devleesschauwer, B.; Michele Cecchini, M.; et al. Attributable deaths and disability-adjusted life-years caused by infections with antibiotic-resistant bacteria in the EU and the European Economic Area in 2015: A population-level modelling analysis. Lancet Infect. Dis. 2019, 19, 56–66. [Google Scholar] [CrossRef]
  6. Dadgostar, P. Antimicrobial Resistance: Implications and Costs. Infect. Drug Resist. 2019, 12, 3903–3910. [Google Scholar] [CrossRef]
  7. Murray, C.J.; Ikuta, K.S.; Sharara, F.; Swetschinski, L.; Aguilar, G.R.; Gray, A.; Han, C.; Bisignano, C.; Rao, P.; Wool, E.; et al. Global burden of bacterial antimicrobial resistance in 2019: A systematic analysis. Lancet 2022, 399, 629–655. [Google Scholar] [CrossRef]
  8. Gautam, A. Antimicrobial Resistance: The Next Probable Pandemic. JNMA J. Nepal Med. Assoc. 2022, 60, 225–228. [Google Scholar] [CrossRef]
  9. Charani, E.; Mendelson, M.; Pallett, S.J.C.; Ahmad, R.; Mpundu, M.; Mbamalu, O.; Bonaconsa, C.; Nampoothiri, V.; Singh, S.; Peiffer-Smadja, N.; et al. An analysis of existing national action plans for antimicrobial resistance-gaps and opportunities in strategies optimising antibiotic use in human populations. Lancet Glob. Health 2023, 11, e466–e474. [Google Scholar] [CrossRef]
  10. Godman, B.; Egwuenu, A.; Wesangula, E.; Schellack, N.; Kalungia, A.C.; Tiroyakgosi, C.; Kgatlwane, J.; Mwita, J.C.; Patrick, O.; Niba, L.L.; et al. Tackling antimicrobial resistance across sub-Saharan Africa: Current challenges and implications for the future. Expert Opin. Drug Saf. 2022, 21, 1089–1111. [Google Scholar] [CrossRef]
  11. Nabadda, S.; Kakooza, F.; Kiggundu, R.; Walwema, R.; Bazira, J.; Mayito, J.; Mugerwa, I.; Sekamatte, M.; Kambugu, A.; Lamorde, M.; et al. Implementation of the World Health Organization Global Antimicrobial Resistance Surveillance System in Uganda, 2015–2020: Mixed-Methods Study Using National Surveillance Data. JMIR Public Health Surveill. 2021, 7, e29954. [Google Scholar] [CrossRef]
  12. WHO Implementation Handbook for National Action Plans on Antimicrobial Resistance: Guidance for the Human Health Sector. 2022. Available online: https://www.who.int/publications/i/item/9789240041981 (accessed on 5 April 2023).
  13. WHO. Global Action Plan on Antimicrobial Resistance—Report by the Secretariat. 2016. Available online: https://apps.who.int/gb/ebwha/pdf_files/WHA69/A69_24-en.pdf (accessed on 5 April 2023).
  14. Sharland, M.; Pulcini, C.; Harbarth, S.; Zeng, M.; Gandra, S.; Mathur, S.; Magrini, N. Classifying antibiotics in the WHO Essential Medicines List for optimal use-be AWaRe. Lancet Infect. Dis. 2018, 18, 18–20. [Google Scholar] [CrossRef]
  15. Sharland, M.; Gandra, S.; Huttner, B.; Moja, L.; Pulcini, C.; Zeng, M.; Mendelson, M.; Cappello, B.; Cooke, G.; Magrini, N.; et al. Encouraging AWaRe-ness and discouraging inappropriate antibiotic use-the new 2019 Essential Medicines List becomes a global antibiotic stewardship tool. Lancet Infect. Dis. 2019, 19, 1278–1280. [Google Scholar] [CrossRef]
  16. WHO. The WHO AWaRe (Access, Watch, Reserve) Antibiotic Book. 2022. Available online: https://www.who.int/publications/i/item/9789240062382 (accessed on 5 April 2023).
  17. Sharland, M.; Zanichelli, V.; Ombajo, L.A.; Bazira, J.; Cappello, B.; Chitatanga, R.; Chuki, P.; Gandra, S.; Getahun, H.; Harbarth, S.; et al. The WHO essential medicines list AWaRe book: From a list to a quality improvement system. Clin. Microbiol. Infect. 2022, 28, 1533–1535. [Google Scholar] [CrossRef] [PubMed]
  18. Sulis, G.; Sayood, S.; Katukoori, S.; Bollam, N.; George, I.; Yaeger, L.H.; Chavez, M.A.; Tetteh, E.; Yarrabelli, S.; Pulcini, C.; et al. Exposure to World Health Organization’s AWaRe antibiotics and isolation of multidrug resistant bacteria: A systematic review and meta-analysis. Clin. Microbiol. Infect. 2022, 28, 1193–1202. [Google Scholar] [CrossRef]
  19. Klein, E.Y.; Milkowska-Shibata, M.; Tseng, K.K.; Sharland, M.; Gandra, S.; Pulcini, C.; Laxminarayan, R. Assessment of WHO antibiotic consumption and access targets in 76 countries, 2000–2015: An analysis of pharmaceutical sales data. Lancet Infect. Dis. 2021, 21, 107–115. [Google Scholar] [CrossRef] [PubMed]
  20. Fürst, J.; Čižman, M.; Mrak, J.; Kos, D.; Campbell, S.; Coenen, S.; Gustafsson, L.L.; Fürst, L.; Godman, B. The influence of a sustained multifaceted approach to improve antibiotic prescribing in Slovenia during the past decade: Findings and implications. Expert Rev. Anti Infect. Ther. 2015, 13, 279–289. [Google Scholar] [CrossRef] [PubMed]
  21. Bojanić, L.; Marković-Peković, V.; Škrbić, R.; Stojaković, N.; Ðermanović, M.; Bojanić, J.; Fürst, J.; Kurdi, A.; Godman, B. Recent Initiatives in the Republic of Srpska to Enhance Appropriate Use of Antibiotics in Ambulatory Care; Their Influence and Implications. Front. Pharmacol. 2018, 9, 442. [Google Scholar] [CrossRef]
  22. Abilova, V.; Kurdi, A.; Godman, B. Ongoing initiatives in Azerbaijan to improve the use of antibiotics; findings and implications. Expert Rev. Anti Infect. Ther. 2018, 16, 77–84. [Google Scholar] [CrossRef]
  23. Robertson, J.; Iwamoto, K.; Hoxha, I.; Ghazaryan, L.; Abilova, V.; Cvijanovic, A.; Pyshnik, H.; Darakhvelidze, M.; Makalkina, L.; Jakupi, A.; et al. Antimicrobial Medicines Consumption in Eastern Europeand Central Asia—An Updated Cross-National Study and Assessment of Quantitative Metrics for Policy Action. Front. Pharmacol. 2018, 9, 1156. [Google Scholar] [CrossRef]
  24. EVIPNet Europe. Tackling Antimicrobial Resistance in Primary Health Care through Promoting the Appropriate Use of Antibiotics in Estonia. 2022. Available online: https://apps.who.int/iris/bitstream/handle/10665/351528/WHO-EURO-2022-4779-44542-63078-eng.pdf (accessed on 8 April 2023).
  25. Ministry of Health Republic of Latvia. Latvia’s Experience on AMR Policy Development. Meeting of the subgroup of the AMR One Health Network on AMR NAPs 31 May 2022–01 June 2022. Available online: https://health.ec.europa.eu/system/files/2022-06/amr_20220531_co10_en.pdf (accessed on 15 April 2023).
  26. Tesar, T.; Masarykova, L.; Lehocka, L.; Porubcova, S.; Cicova, M.; Wawruch, M. Consumption of Antibacterials for Systemic Use in Slovakia: A National Study and the Quality Indicators for Outpatient Antibiotic Use. Antibiotics 2021, 10, 1180. [Google Scholar] [CrossRef]
  27. Wojkowska-Mach, J.; Godman, B.; Glassman, A.; Kurdi, A.; Pilc, A.; Rozanska, A.; Skoczyński, S.; Wałaszek, M.; Bochenek, T. Antibiotic consumption and antimicrobial resistance in Poland; findings and implications. Antimicrob. Resist. Infect. Control 2018, 7, 136. [Google Scholar] [CrossRef]
  28. Rolfe, R., Jr.; Kwobah, C.; Muro, F.; Ruwanpathirana, A.; Lyamuya, F.; Bodinayake, C.; Nagahawatte, A.; Piyasiri, B.; Sheng, T.; Bollinger, J.; et al. Barriers to implementing antimicrobial stewardship programs in three low- and middle-income country tertiary care settings: Findings from a multi-site qualitative study. Antimicrob. Resist. Infect. Control 2021, 10, 60. [Google Scholar] [CrossRef]
  29. Bosley, H.; Henshall, C.; Appleton, J.V.; Jackson, D. A systematic review to explore influences on parental attitudes towards antibiotic prescribing in children. J. Clin. Nurs. 2018, 27, 892–905. [Google Scholar] [CrossRef]
  30. Kenyon, C.; Manoharan-Basil, S.S. Cultural Drivers of Antibiotic Consumption in High-Income Countries: A Global Ecological Analysis. Microb. Drug Resist. 2020, 26, 1063–1070. [Google Scholar] [CrossRef]
  31. Borg, M.A.; Camilleri, L. Broad-spectrum antibiotic use in Europe: More evidence of cultural influences on prescribing behaviour. J. Antimicrob. Chemother. 2019, 74, 3379–3383. [Google Scholar] [CrossRef]
  32. Maugeri, A.; Barchitta, M.; Puglisi, F.; Agodi, A. Socio-economic, governance and health indicators shaping antimicrobial resistance: An ecological analysis of 30 european countries. Glob. Health 2023, 19, 12. [Google Scholar] [CrossRef]
  33. Mueller, T.; Östergren, P.O. The correlation between regulatory conditions and antibiotic consumption within the WHO European Region. Health Policy 2016, 120, 882–889. [Google Scholar] [CrossRef]
  34. Collignon, P.; Athukorala, P.C.; Senanayake, S.; Khan, F. Antimicrobial resistance: The major contribution of poor governance and corruption to this growing problem. PLoS ONE 2015, 10, e0116746. [Google Scholar] [CrossRef]
  35. Rönnerstrand, B.; Lapuente, V. Corruption and use of antibiotics in regions of Europe. Health Policy 2017, 121, 250–256. [Google Scholar] [CrossRef]
  36. INSTAT. Annual Average of Total Population by Age_Group, Gender, Type and Year—Albania. 2023. Available online: http://databaza.instat.gov.al/pxweb/en/DST/START__DE/NewPOP_0001/table/tableViewLayout1/ (accessed on 4 April 2023).
  37. Transparency International. Corruption Perceptions Index. Albania. 2022. Available online: https://www.transparency.org/en/cpi/2022/index/alb (accessed on 4 April 2023).
  38. Hoxha, I.; Malaj, A.; Kraja, B.; Bino, S.; Oluka, M.; Marković-Peković, V.; Godman, B. Are pharmacists’ good knowledge and awareness on antibiotics taken for granted? The situation in Albania and future implications across countries. J. Glob. Antimicrob. Resist. 2018, 13, 240–245. [Google Scholar] [CrossRef]
  39. Kleva, S.; Elona, K.; Edit, X.; Anis, T.; Neada, H.; Suida, K. Approach to the Current Rational Use of Antibiotics among the Albanian Dentist Community. J. Pharm. Bioallied Sci. 2022, 14, 106–113. [Google Scholar] [CrossRef]
  40. WHO. Joint External Evaluation of IHR Core Capacities of the Republic of Albania—Mission Report: September 2016. Available online: https://www.who.int/countries/alb/ (accessed on 4 April 2023).
  41. Hoxha, I.; Malaj, A.; Tako, R.; Malaj, L. Survey on how antibiotics are dispensed in community pharmacies in Albania. Int. J. Pharm. Pharm. Sci. 2015, 7, 449–450. [Google Scholar]
  42. Kaae, S.; Malaj, A.; Hoxha, I. Antibiotic knowledge, attitudes and behaviours of Albanian health care professionals and patients—A qualitative interview study. J. Pharm. Policy Pract. 2017, 10, 13. [Google Scholar] [CrossRef] [PubMed]
  43. Marković-Peković, V.; Grubiša, N.; Burger, J.; Bojanić, L.; Godman, B. Initiatives to Reduce Nonprescription Sales and Dispensing of Antibiotics: Findings and Implications. J. Res. Pharm. Pract. 2017, 6, 120–125. [Google Scholar] [PubMed]
  44. Nika, D.; Zarb, P. Antimicrobial consumption in Albanian reference teaching hospital (2012–2015). J. Infect. Dev. Ctries. 2017, 11, 517–520. [Google Scholar] [CrossRef] [PubMed]
  45. Robertson, J.; Vlahović-Palčevski, V.; Iwamoto, K.; Högberg, L.D.; Godman, B.; Monnet, D.L.; Garner, S.; Weist, K.; ESAC-Net Study Group; WHO Europe AMC Network Study Group. Variations in the Consumption of Antimicrobial Medicines in the European Region, 2014–2018: Findings and Implications from ESAC-Net and WHO Europe. Front. Pharmacol. 2021, 12, 639207. [Google Scholar] [CrossRef] [PubMed]
  46. Hoxha, I.; Malaj, A.; Malaj, L. Antibiotic use in Albania between 2011 and 2012. J. Infect. Dev. Ctries. 2015, 9, 94–98. [Google Scholar] [CrossRef] [PubMed]
  47. WHO. Albania: National Action Plan against Antimicrobial Resistance 2017. 25 November 2022. Available online: https://cdn.who.int/media/docs/default-source/antimicrobial-resistance/amr-spc-npm/nap-library/albania-amr-nap-2017.pdf?sfvrsn=8ba07901_3&download=true (accessed on 6 April 2023).
  48. Bednarčuk, N.; Golić Jelić, A.; Stoisavljević Šatara, S.; Stojaković, N.; Marković Peković, V.; Stojiljković, M.P.; Popović, N.; Škrbić, R. Antibiotic Utilization during COVID-19: Are We Over-Prescribing? Antibiotics 2023, 12, 308. [Google Scholar] [CrossRef] [PubMed]
  49. Khan, S.; Hasan, S.S.; Bond, S.E.; Conway, B.R.; Aldeyab, M.A. Antimicrobial consumption in patients with COVID-19: A systematic review and meta-analysis. Expert Rev. Anti Infect. Ther. 2022, 20, 749–772. [Google Scholar] [CrossRef] [PubMed]
  50. Langford, B.J.; So, M.; Raybardhan, S.; Leung, V.; Soucy, J.R.; Westwood, D.; Daneman, N.; MacFadden, D.R. Antibiotic prescribing in patients with COVID-19: Rapid review and meta-analysis. Clin. Microbiol. Infect. 2021, 27, 520–531. [Google Scholar] [CrossRef] [PubMed]
  51. Alshaikh, F.S.; Godman, B.; Sindi, O.N.; Seaton, R.A.; Kurdi, A. Prevalence of bacterial coinfection and patterns of antibiotics prescribing in patients with COVID-19: A systematic review and meta-analysis. PLoS ONE 2022, 17, e0272375. [Google Scholar] [CrossRef]
  52. Nandi, A.; Pecetta, S.; Bloom, D.E. Global antibiotic use during the COVID-19 pandemic: Analysis of pharmaceutical sales data from 71 countries, 2020–2022. eClinicalMedicine 2023, 57, 101848. [Google Scholar] [CrossRef]
  53. Sulis, G.; Batomen, B.; Kotwani, A.; Pai, M.; Gandra, S. Sales of antibiotics and hydroxychloroquine in India during the COVID-19 epidemic: An interrupted time series analysis. PLoS Med 2021, 18, e1003682. [Google Scholar] [CrossRef]
  54. World Bank. GDP per Capita (US$). 2021. Available online: https://data.worldbank.org/indicator/NY.GDP.PCAP.CD (accessed on 7 April 2023).
  55. Zanichelli, V.; Sharland, M.; Cappello, B.; Moja, L.; Getahun, H.; Pessoa-Silva, C.; Sati, H.; van Weezenbeek, C.; Balkhy, H.; Simão, M.; et al. The WHO AWaRe (Access, Watch, Reserve) antibiotic book and prevention of antimicrobial resistance. Bull. World Health Organ. 2023, 101, 290–296. [Google Scholar] [CrossRef]
  56. Godman, B.; Haque, M.; McKimm, J.; Abu Bakar, M.; Sneddon, J.; Wale, J.; Campbell, S.; Martin, A.P.; Hoxha, I.; Abilova, V.; et al. Ongoing strategies to improve the management of upper respiratory tract infections and reduce inappropriate antibiotic use particularly among lower and middle-income countries: Findings and implications for the future. Curr. Med. Res. Opin. 2020, 36, 301–327. [Google Scholar] [CrossRef]
  57. Collignon, P.; Beggs, J.J.; Walsh, T.R.; Gandra, S.; Laxminarayan, R. Anthropological and socioeconomic factors contributing to global antimicrobial resistance: A univariate and multivariable analysis. Lancet Planet Health 2018, 2, e398–e405. [Google Scholar] [CrossRef]
  58. Mwita, J.C.; Ogunleye, O.O.; Olalekan, A.; Kalungia, A.C.; Kurdi, A.; Saleem, Z.; Sneddon, J.; Godman, B. Key Issues Surrounding Appropriate Antibiotic Use for Prevention of Surgical Site Infections in Low- and Middle-Income Countries: A Narrative Review and the Implications. Int. J. Gen. Med. 2021, 14, 515–530. [Google Scholar] [CrossRef]
  59. Saleem, Z.; Ahsan, U.; Haseeb, A.; Altaf, U.; Batool, N.; Rani, H.; Jaffer, J.; Shahid, F.; Hussain, M.; Amir, A.; et al. Antibiotic Utilization Patterns for Different Wound Types among Surgical Patients: Findings and Implications. Antibiotics 2023, 12, 678. [Google Scholar] [CrossRef]
  60. Cox, J.A.; Vlieghe, E.; Mendelson, M.; Wertheim, H.; Ndegwa, L.; Villegas, M.V.; Gould, I.; Hara, G.L. Antibiotic stewardship in low- and middle-income countries: The same but different? Clin. Microbiol. Infect. 2017, 23, 812–818. [Google Scholar] [CrossRef]
  61. GolAli, E.; Sistanizad, M.; Salamzadeh, J.; Haghighi, M.; Solooki, M. Antibiotic Prescribing Trends Before and After Implementation of an Audit and Feedback Program in Internal Ward of a Tertiary Hospital in Tehran. Iran J. Pharm. Res. 2019, 18, 2136–2143. [Google Scholar]
  62. Dellsperger, S.; Kramer, S.; Stoller, M.; Burger, A.; Geissbühler, E.; Amsler, I.; Hirsig, A.; Weyer, L.; Hebeisen, U.; Aebi, P.; et al. Early Switch from Intravenous to Oral Antibiotics in Skin and Soft Tissue Infections: An Algorithm-Based Prospective Multicenter Pilot Trial. Open Forum Infect. Dis. 2022, 9, ofac197. [Google Scholar] [CrossRef]
  63. Mustafa, Z.U.; Khan, A.H.; Harun, S.N.; Salman, M.; Godman, B. Antibiotic Overprescribing among Neonates and Children Hospitalized with COVID-19 in Pakistan and the Implications. Antibiotics 2023, 12, 646. [Google Scholar] [CrossRef]
  64. Langford, B.J.; So, M.; Raybardhan, S.; Leung, V.; Westwood, D.; MacFadden, D.R.; Soucy, J.-P.R.; Daneman, N. Bacterial co-infection and secondary infection in patients with COVID-19: A living rapid review and meta-analysis. Clin. Microbiol. Infect. 2020, 26, 1622–1629. [Google Scholar] [CrossRef] [PubMed]
  65. Mukokinya, M.M.A.; Opanga, S.; Oluka, M.; Godman, B. Dispensing of Antimicrobials in Kenya: A Cross-sectional Pilot Study and Its Implications. J. Res. Pharm. Pract. 2018, 7, 77–82. [Google Scholar] [PubMed]
  66. Opanga, S.R.N.; Wamaitha, A.; Abebrese Sefah, I.; Godman, B.B. Availability of Medicines in Community Pharmacy to Manage Patients with COVID-19 in Kenya; Pilot Study and Implications. Sch. Acad. J. Pharm. 2021, 3, 36–42. [Google Scholar] [CrossRef]
  67. Kibuule, D.N.L.; Sefah, I.A.; Kurdi, A.; Phuong, T.N.T.; Kwon, H.-Y.; Godman, B. Activities in Namibia to limit the prevalence and mortality from COVID-19 including community pharmacy activities and the implications. Sch. Acad. J. Pharm. 2021, 5, 82–92. [Google Scholar] [CrossRef]
  68. WHO Regional Office for Europe Antimicrobial Medicines Consumption (AMC) Network. AMC Data 2019. Copenhagen: WHO Regional Office for Europe. 2022. Available online: https://apps.who.int/iris/bitstream/handle/10665/363394/9789289058278-eng.pdf?sequence=1&isAllowed=y (accessed on 7 April 2023).
  69. Versporten, A.; Bolokhovets, G.; Ghazaryan, L.; Abilova, V.; Pyshnik, G.; Spasojevic, T.; Korinteli, I.; Raka, L.; Kambaralieva, B.; Cizmovic, L.; et al. Antibiotic use in eastern Europe: A cross-national database study in coordination with the WHO Regional Office for Europe. Lancet Infect. Dis. 2014, 14, 381–387. [Google Scholar] [CrossRef]
  70. WHO. Anatomical Therapeutic Chemical (ATC) Classification. 2021. Available online: https://www.who.int/tools/atc-ddd-toolkit/atc-classification (accessed on 25 March 2023).
  71. Tang, Y.; Liu, C.; Zhang, Z.; Zhang, X. Effects of prescription restrictive interventions on antibiotic procurement in primary care settings: A controlled interrupted time series study in China. Cost Eff. Resour. Alloc. 2018, 16, 1. [Google Scholar] [CrossRef]
  72. Hider-Mlynarz, K.; Cavalié, P.; Maison, P. Trends in analgesic consumption in France over the last 10 years and comparison of patterns across Europe. Br. J. Clin. Pharmacol. 2018, 84, 1324–1334. [Google Scholar] [CrossRef]
  73. Godman, B.; Egwuenu, A.; Haque, M.; Malande, O.O.; Schellack, N.; Kumar, S.; Saleem, Z.; Sneddon, J.; Hoxha, I.; Islam, S.; et al. Strategies to Improve Antimicrobial Utilization with a Special Focus on Developing Countries. Life 2021, 11, 528. [Google Scholar] [CrossRef]
  74. Oppong, R.; Smith, R.D.; Little, P.; Verheij, T.; Butler, C.C.; Goossens, H.; Coenen, S.; Jowett, S.; Roberts, T.E.; Achana, F.; et al. Cost-effectiveness of internet-based training for primary care clinicians on antibiotic prescribing for acute respiratory tract infections in Europe. J. Antimicrob. Chemother. 2018, 73, 3189–3198. [Google Scholar] [CrossRef]
  75. Oppong, R.; Smith, R.D.; Little, P.; Verheij, T.; Butler, C.C.; Goossens, H.; Coenen, S.; Moore, M.; Coast, J. Cost effectiveness of amoxicillin for lower respiratory tract infections in primary care: An economic evaluation accounting for the cost of antimicrobial resistance. Br. J. Gen. Pract. 2016, 66, e633–e639. [Google Scholar] [CrossRef] [PubMed]
  76. Lambert, M.; Smit, C.C.H.; De Vos, S.; Benko, R.; Llor, C.; Paget, W.J.; Briant, K.; Pont, L.; Van Dijk, L.; Taxis, K.; et al. A systematic literature review and meta-analysis of community pharmacist-led interventions to optimise the use of antibiotics. Br. J. Clin. Pharmacol. 2022, 88, 2617–2641. [Google Scholar] [CrossRef]
  77. Parveen, S.; Garzon-Orjuela, N.; Amin, D.; McHugh, P.; Vellinga, A. Public Health Interventions to Improve Antimicrobial Resistance Awareness and Behavioural Change Associated with Antimicrobial Use: A Systematic Review Exploring the Use of Social Media. Antibiotics 2022, 11, 669. [Google Scholar] [CrossRef] [PubMed]
  78. Allegranzi, B.; Aiken, A.M.; Zeynep Kubilay, N.; Nthumba, P.; Barasa, J.; Okumu, G.; Mugarura, R.; Elobu, A.; Jombwe, J.; Maimbo, M.; et al. A multimodal infection control and patient safety intervention to reduce surgical site infections in Africa: A multicentre, before-after, cohort study. Lancet Infect. Dis. 2018, 18, 507–515. [Google Scholar] [CrossRef]
  79. Saied, T.; Hafez, S.F.; Kandeel, A.; El-kholy, A.; Ismail, G.; Aboushady, M.; Attia, E.; Hassaan, A.; Abdel-Atty, O.; Elfekky, E.; et al. Antimicrobial stewardship to optimize the use of antimicrobials for surgical prophylaxis in Egypt: A multicenter pilot intervention study. Am. J. Infect. Contro. 2015, 43, e67–e71. [Google Scholar] [CrossRef]
  80. Shankar, R. Implementation of the WHO Surgical Safety Checklist at a teaching hospital in India and evaluation of the effects on perioperative complications. Int. J. Health Plan. Manag. 2018, 33, 836–846. [Google Scholar] [CrossRef]
  81. Mahmoudi, L.; Ghouchani, M.; Mahi-Birjand, M.; Bananzadeh, A.; Akbari, A. Optimizing compliance with surgical antimicrobial prophylaxis guidelines in patients undergoing gastrointestinal surgery at a referral teaching hospital in southern Iran: Clinical and economic impact. Infect. Drug Resist. 2019, 12, 2437–2444. [Google Scholar] [CrossRef]
  82. Aiken, A.M.; Wanyoro, A.K.; Mwangi, J.; Juma, F.; Mugoya, I.K.; Scott, J.A. Changing use of surgical antibiotic prophylaxis in Thika Hospital, Kenya: A quality improvement intervention with an interrupted time series design. PLoS ONE 2013, 8, e78942. [Google Scholar] [CrossRef]
  83. Ntumba, P.; Mwangi, C.; Barasa, J.; Aiken, A.; Kubilay, Z.; Allegranzi, B. Multimodal approach for surgical site infection prevention—Results from a pilot site in Kenya. Antimicrob. Resist. Infect. Control. 2015, 4, P87. [Google Scholar] [CrossRef]
  84. Kim, R.Y.; Kwakye, G.; Kwok, A.C.; Baltaga, R.; Ciobanu, G.; Merry, A.F.; Funk, L.M.; Lipsitz, S.R.; Gawande, A.A.; Berry, W.R.; et al. Sustainability and long-term effectiveness of the WHO surgical safety checklist combined with pulse oximetry in a resource-limited setting: Two-year update from Moldova. JAMA Surg. 2015, 150, 473–479. [Google Scholar] [CrossRef]
  85. Abubakar, U.; Syed Sulaiman, S.A.; Adesiyun, A.G. Impact of pharmacist-led antibiotic stewardship interventions on compliance with surgical antibiotic prophylaxis in obstetric and gynecologic surgeries in Nigeria. PLoS ONE 2019, 14, e0213395. [Google Scholar] [CrossRef] [PubMed]
  86. Butt, S.Z.; Ahmad, M.; Saeed, H.; Saleem, Z.; Javaid, Z. Post-surgical antibiotic prophylaxis: Impact of pharmacist’s educational intervention on appropriate use of antibiotics. J. Infect. Public Health 2019, 12, 854–860. [Google Scholar] [CrossRef] [PubMed]
  87. Brink, A.J.; Messina, A.P.; Feldman, C.; Richards, G.A.; van den Bergh, D. From guidelines to practice: A pharmacist-driven prospective audit and feedback improvement model for peri-operative antibiotic prophylaxis in 34 South African hospitals. J. Antimicrob. Chemother. 2017, 72, 1227–1234. [Google Scholar] [CrossRef] [PubMed]
  88. Bozkurt, F.; Kaya, S.; Tekin, R.; Gulsun, S.; Deveci, O.; Dayan, S.; Hoşoglu, S. Analysis of antimicrobial consumption and cost in a teaching hospital. J. Infect. Public Health 2014, 7, 161–169. [Google Scholar] [CrossRef]
  89. Karaali, C.; Emiroglu, M.; Atalay, S.; Sert, I.; Dursun, A.; Kose, S.; Akbulut, G.; Aydın, C.A. A new antibiotic stewardship program approach is effective on inappropriate surgical prophylaxis and discharge prescription. J. Infect. Dev. Ctries. 2019, 13, 961–967. [Google Scholar] [CrossRef]
  90. Teng, C.L.; Achike, F.I.; Phua, K.L.; Nurjahan, M.I.; Mastura, I.; Asiah, H.N.; Mariam, A.M.; Narayanan, S.; Norsiah, A.; Sabariah, I.; et al. Modifying antibiotic prescribing: The effectiveness of academic detailing plus information leaflet in a Malaysian primary care setting. Med. J. Malays. 2006, 61, 323–331. [Google Scholar]
  91. Awad, A.I.; Eltayeb, I.B.; Baraka, O.Z. Changing antibiotics prescribing practices in health centers of Khartoum State, Sudan. Eur. J. Clin. Pharmacol. 2006, 62, 135–142. [Google Scholar] [CrossRef]
  92. Chowdhury, A.K.; Khan, O.F.; Matin, M.A.; Begum, K.; Galib, M.A. Effect of standard treatment guidelines with or without prescription audit on prescribing for acute respiratory tract infection (ARI) and diarrhoea in some thana health complexes (THCs) of Bangladesh. Bangladesh Med. Res. Counc. Bull. 2007, 33, 21–30. [Google Scholar]
  93. Kafle, K.K.; Bhuju, G.B.; Karkee, S.B.; Prasad, R.R.; Shrestha, N.; Shrestha, A.D.; Das, P.L.; Chataut, B.D.; Daud, M. An intervention improving prescribing practices and monitoring drugs availability in a district. Nepal Med. Coll. J. 2009, 11, 217–221. [Google Scholar]
  94. Yip, W.; Powell-Jackson, T.; Chen, W.; Hu, M.; Fe, E.; Hu, M.; Hsiao, W.C. Capitation combined with pay-for-performance improves antibiotic prescribing practices in rural China. Health Aff. 2014, 33, 502–510. [Google Scholar] [CrossRef]
  95. Boonyasiri, A.; Thamlikitkul, V. Effectiveness of multifaceted interventions on rational use of antibiotics for patients with upper respiratory tract infections and acute diarrhea. J. Med. Assoc. Thail. 2014, 97 (Suppl. 3), S13–S19. [Google Scholar]
  96. Egger, J.R.; Stankevitz, K.; Korom, R.; Angwenyi, P.; Sullivan, B.; Wang, J.; Hatfield, S.; Smith, E.; Popli, K.; Gross, J. Evaluating the effects of organizational and educational interventions on adherence to clinical practice guidelines in a low-resource primary-care setting in Kenya. Health Policy Plan. 2017, 32, 761–768. [Google Scholar] [CrossRef] [PubMed]
  97. Korom, R.R.; Onguka, S.; Halestrap, P.; McAlhaney, M.; Adam, M. Brief educational interventions to improve performance on novel quality metrics in ambulatory settings in Kenya: A multi-site pre-post effectiveness trial. PLoS ONE 2017, 12, e0174566. [Google Scholar] [CrossRef] [PubMed]
  98. Dehn Lunn, A. Reducing inappropriate antibiotic prescribing in upper respiratory tract infection in a primary care setting in Kolkata, India. BMJ Open Qual. 2018, 7, e000217. [Google Scholar] [CrossRef]
  99. Tay, K.H.; Ariffin, F.; Sim, B.L.; Chin, S.Y.; Sobry, A.C. Multi-Faceted Intervention to Improve the Antibiotic Prescriptions among Doctors for Acute URI and Acute Diarrhoea Cases: The Green Zone Antibiotic Project. Malays. J. Med. Sci. MJMS 2019, 26, 101–109. [Google Scholar] [CrossRef]
  100. Brinkmann, I.; Kibuule, D. Effectiveness of antibiotic stewardship programmes in primary health care settings in developing countries. Res. Soc. Adm. Pharm. 2020, 16, 1309–1313. [Google Scholar] [CrossRef]
  101. Chalker, J.; Ratanawijitrasin, S.; Chuc, N.T.; Petzold, M.; Tomson, G. Effectiveness of a multi-component intervention on dispensing practices at private pharmacies in Vietnam and Thailand--a randomized controlled trial. Soc. Sci. Med. 2005, 60, 131–141. [Google Scholar] [CrossRef]
  102. Nguyen, T.T.P.; Do, T.X.; Nguyen, H.A.; Nguyen, C.T.T.; Meyer, J.C.; Godman, B.; Skosana, P.; Nguyen, B.T. A National Survey of Dispensing Practice and Customer Knowledge on Antibiotic Use in Vietnam and the Implications. Antibiotics 2022, 11, 1091. [Google Scholar] [CrossRef]
  103. Santa-Ana-Tellez, Y.; Mantel-Teeuwisse, A.K.; Dreser, A.; Leufkens, H.G.; Wirtz, V.J. Impact of over-the-counter restrictions on antibiotic consumption in Brazil and Mexico. PLoS ONE 2013, 8, e75550. [Google Scholar] [CrossRef]
  104. Santa-Ana-Tellez, Y.; Mantel-Teeuwisse, A.K.; Leufkens, H.G.M.; Wirtz, V.J. Seasonal Variation in Penicillin Use in Mexico and Brazil: Analysis of the Impact of Over-the-Counter Restrictions. Antimicrob. Agents Chemother. 2015, 59, 105–110. [Google Scholar] [CrossRef]
  105. Arparsrithongsagul, S.; Kulsomboon, V.; Zuckerman, I.H. Multidisciplinary perspective intervention with community involvement to decrease antibiotic sales in village groceries in Thailand. Asia Pac. J. Public Health 2015, 27, Np2480-8. [Google Scholar] [CrossRef] [PubMed]
  106. Kitutu, F.E.; Kalyango, J.N.; Mayora, C.; Selling, K.E.; Peterson, S.; Wamani, H. Integrated community case management by drug sellers influences appropriate treatment of paediatric febrile illness in South Western Uganda: A quasi-experimental study. Malar. J. 2017, 16, 425. [Google Scholar] [CrossRef] [PubMed]
  107. Kimathi, G.; Kiarie, J.; Njarambah, L.; Onditi, J.; Ojakaa, D. A cross-sectional study of antimicrobial use among self-medicating COVID-19 cases in Nyeri County, Kenya. Antimicrob. Resist. Infect. Control 2022, 11, 111. [Google Scholar] [CrossRef]
  108. Muloi, D.; Fèvre, E.M.; Bettridge, J.; Rono, R.; Ong’are, D.; Hassell, J.M.; Karani, M.K.; Muinde, P.; van Bunnik, B.; Street, A.; et al. A cross-sectional survey of practices and knowledge among antibiotic retailers in Nairobi, Kenya. J. Glob. Health 2019, 9, 010412. [Google Scholar] [CrossRef] [PubMed]
  109. WHO. Kenya National Action Plan on Antimicrobial Resistance: Review of Progress in the Human Health Sector. 2022. Available online: https://www.who.int/publications/i/item/9789240062689 (accessed on 5 April 2023).
  110. Chang, J.; Xu, S.; Zhu, S.; Li, Z.; Yu, J.; Zhang, Y.; Zu, J.; Fang, Y.; Ross-Degnan, D. Assessment of non-prescription antibiotic dispensing at community pharmacies in China with simulated clients: A mixed cross-sectional and longitudinal study. Lancet Infect. Dis. 2019, 19, 1345–1354. [Google Scholar] [CrossRef]
  111. Sefah, I.A.; Ogunleye, O.O.; Essah, D.O.; Opanga, S.A.; Butt, N.; Wamaitha, A.; Guantai, A.N.; Chikowe, I.; Khuluza, F.; Kibuule, D.; et al. Rapid Assessment of the Potential Paucity and Price Increases for Suggested Medicines and Protection Equipment for COVID-19 Across Developing Countries with a Particular Focus on Africa and the Implications. Front. Pharmacol. 2020, 11, 588106. [Google Scholar] [CrossRef]
  112. Kamati, M.; Godman, B.; Kibuule, D. Prevalence of self-medication for acute respiratory infections in young children in Namibia: Findings and implications. J. Res. Pharm. Pract. 2019, 8, 220. [Google Scholar]
  113. Onwunduba, A.; Ekwunife, O.; Onyilogwu, E. Impact of point-of-care C-reactive protein testing intervention on non-prescription dispensing of antibiotics for respiratory tract infections in private community pharmacies in Nigeria: A cluster randomized controlled trial. Int. J. Infect. Dis. 2023, 127, 137–143. [Google Scholar] [CrossRef]
Antibiotics 12 00882 g001 550
Figure 1. Trends in antibiotic utilization 2011–2021. NB: ‘Watch’ antibiotics based on the AWaRe classification [14,15]—See Section 4 for details.
Figure 1. Trends in antibiotic utilization 2011–2021. NB: ‘Watch’ antibiotics based on the AWaRe classification [14,15]—See Section 4 for details.
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Antibiotics 12 00882 g002 550
Figure 2. ‘Watch’ antibiotics as percentage of the top 10 most utilized antibiotics 2011—2021.
Figure 2. ‘Watch’ antibiotics as percentage of the top 10 most utilized antibiotics 2011—2021.
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Figure 3. Scatterplots of antibiotic consumption vs. other factors in Albania. (a) Antibiotic consumption vs. median age of Albanian population 2011–2021. (b) Antibiotic consumption vs. GDP per capita in Albania 2011–2021. (c) Antibiotic consumption vs. corruption index score of Albania 2011–2021.
Figure 3. Scatterplots of antibiotic consumption vs. other factors in Albania. (a) Antibiotic consumption vs. median age of Albanian population 2011–2021. (b) Antibiotic consumption vs. GDP per capita in Albania 2011–2021. (c) Antibiotic consumption vs. corruption index score of Albania 2011–2021.
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Table
Table 1. Top 10 most used antibiotics in Albania expressed in DID from 2011 up to 2021.
Table 1. Top 10 most used antibiotics in Albania expressed in DID from 2011 up to 2021.
2011DID2012DID2013DID2014DID2015DID2016DID2018DID2018DID2019DID2020DID2021DID
Tetracycline6.5Amoxicillin6.0Amoxicillin3.9Amoxicillin5.8Amoxicillin3.1Co-amoxiclav3.9Co-amoxiclav 3.4Co-amoxiclav2.6Co-amoxiclav2.3Azithromycin3.0Azithromycin4.3
Amoxicillin5.5 Co-amoxiclav3.4Co-amoxiclav 3.4Co-amoxiclav 3.4Ciprofloxacin2.4Cefuroxime1.9Amoxicillin2.8Cefuroxime1.9Cefuroxime2.0Co-amoxiclav 2.7Levofloxacin2.7
Co-amoxiclav2.4Metronidazole3.2Ciprofloxacin1.7Tetracycline2.1Co-amoxiclav 2.0Amoxicillin1.7Cefuroxime2.2Amoxicillin1.8Azithromycin1.9Levofloxacin1.4Co-amoxiclav 2.1
Ciprofloxacin1.3Ciprofloxacin1.9Tetracycline1.2Ciprofloxacin1.7Tetracycline1.6Tetracycline1.6Ciprofloxacin2.0Ciprofloxacin1.8Cefaclor1.5Cefuroxime1.4Ciprofloxacin1.5
Doxycycline1.3Moxifloxacin1.2Doxycycline1.2Doxycycline1.1Cefuroxime1.3Ciprofloxacin1.4Doxycycline1.5Tetracycline1.6Ciprofloxacin1.2Ceftriaxone1.4Cefixime1.5
Cefazolin1.1Azithromycin0.9Azithromycin1.0Cefuroxime1.0Azithromycin1.3Azithromycin1.4Azithromycin1.2Cefaclor1.5Amoxicillin1.1Amoxicillin1.2Ceftriaxone1.4
Cotrimoxazole0.9Cefaclor0.9Cefuroxime0.8Azithromycin1.0Cefixime0.8Clarithromycin1.1Ceftriaxone0.9Azithromycin1.3Levofloxacin1.1Tetracycline1.2Cefuroxime1.2
Moxifloxacin0.9Cefalexin0.8Clarithromycin0.7Clarithromycin0.8Doxycycline0.8Doxycycline0.9Clarithromycin0.8Cefixime1.0Ceftriaxone1.1Ciprofloxacin0.9Tetracycline1.0
Cefaclor0.8Cotrimoxazole0.8Ampicillin0.7Ampicillin0.6Clarithromycin0.6Ceftriaxone0.8Cefixime0.8Levofloxacin1.0Cefixime1.0Cefixime0.8Clarithromycin0.9
Ampicillin0.7Doxycycline0.7Cotrimoxazole0.5Ceftriaxone0.5Nitrofurantoin0.6Levofloxacin0.7Nitrofurantoin0.7Ceftriaxone0.8Doxycycline0.8Cefaclor0.7Cefaclor0.9
Total21.4 19.9 15.2 17.9 14.5 15.4 16.3 15.3 14.0 14.6 17.5
Grand Total27.4 25.7 19.0 22.7 21.0 22.4 22.6 19.0 18.8 21.2 25.1
NB: Antibiotics in the ‘Access’ list are in green, and those in the ‘Watch’ list are in Red. ‘Access’ and ‘Watch’ antibiotics are based on the AWaRe classification [14,15]. See Section 4 for details.
Table
Table 2. Antibiotic utilization and other potential factors.
Table 2. Antibiotic utilization and other potential factors.
YearAntibiotic Utilization (DIDs) *Median Age (Years)GDP per Capita (ALL) *Albania Corruption Index Score *
201127.4032.60447,68933
201225.7033.20459,52631
201319.0033.70466,32533
201422.7034.20482,95431
201521.0034.70497,90233
201622.4035.20511,97136
201722.6035.60539,64539
201819.0036.10571,01138
201918.8036.70592,77936
202021.2037.20580,52135
202125.1037.60660,16836
NB: * Data from [36,37,54]; DDDs per 1000 inhabitants per day; ALL = Albanian Lek.
Table
Table 3. Correlations between antibiotic utilization and potential factors.
Table 3. Correlations between antibiotic utilization and potential factors.
YearsAntibiotic Utilization (DIDs) VS:Kendall’s Tau-b Correlation Coefficientp-Value
(2-Tailed)		95% Confidence Intervals (2-Tailed) a
LowerUpper
2011–2020Median age (years)−0.494 *0.048−0.756−0.098
GDP per capita (ALL)−0.539 *0.031−0.781−0.158
Albania corruption index score−0.2620.312−0.6630.255
2011–2021Median age (years)−0.2940.212−0.6600.185
GDP per capita (ALL)−0.3300.160−0.6820.146
Albania corruption index score−0.2160.378−0.6100.264
NB: DIDs = DDDs per 1000 inhabitants per day; ALL = Albanian Lek. a Estimation is based on Fisher’s r-to-z transformation. * Correlation is significant at the 0.05 level (2-tailed).
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Hoxha, I.; Godman, B.; Malaj, A.; Meyer, J.C. 11-Year Trend in Antibiotic Consumption in a South-Eastern European Country; the Situation in Albania and the Implications for the Future. Antibiotics 2023, 12, 882. https://doi.org/10.3390/antibiotics12050882

AMA Style

Hoxha I, Godman B, Malaj A, Meyer JC. 11-Year Trend in Antibiotic Consumption in a South-Eastern European Country; the Situation in Albania and the Implications for the Future. Antibiotics. 2023; 12(5):882. https://doi.org/10.3390/antibiotics12050882

Chicago/Turabian Style

Hoxha, Iris, Brian Godman, Admir Malaj, and Johanna C. Meyer. 2023. "11-Year Trend in Antibiotic Consumption in a South-Eastern European Country; the Situation in Albania and the Implications for the Future" Antibiotics 12, no. 5: 882. https://doi.org/10.3390/antibiotics12050882

APA Style

Hoxha, I., Godman, B., Malaj, A., & Meyer, J. C. (2023). 11-Year Trend in Antibiotic Consumption in a South-Eastern European Country; the Situation in Albania and the Implications for the Future. Antibiotics, 12(5), 882. https://doi.org/10.3390/antibiotics12050882

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