A decade of antibacterial drug consumption for systemic use in Montenegro (2014–2023): trends, patterns, and AWaRe classification insights
Abstract
Background/Aim. Antimicrobial resistance (AMR) represents an increasing threat to global health, with serious implications for public health and the economy. Monitoring antibiotic consumption is crucial in understanding and addressing AMR. The aim of this study was to analyze trends in the use of antibacterial drugs for systemic use in Montenegro from 2014 to 2023. Methods. A ten-year retrospective study was conducted using data collected by the Institute for Medicines and Medical Devices of Montenegro, Podgorica, Montenegro. Antibiotics were classified according to the World Health Organization’s (WHO) Anatomical Therapeutic Chemical system, expressed in defined daily doses per 1,000 inhabitants per day, and categorized by WHO’s Access, Watch, Reserve (AWaRe) classification to identify trends and patterns in antibiotic use. Results. A gradual decline in antibiotic consumption was observed until 2019, after which a sharp increase in both use and costs occurred during the coronavirus disease 2019 pandemic (2020–2021). Although consumption stabilized after the pandemic, it remained higher compared to pre-pandemic levels. The overall consumption trend showed a tendency to decrease but without statistical significance (p = 0.291), while the increase in costs was also not statistically significant (p = 0.089). The subgroup analysis revealed no significant changes in the antibiotic consumption of J01C and J01M classes. On the other hand, a statistically significant increase was recorded in the use of antibiotics from classes J01D and P01AB (p = 0.001 for both). According to the AWaRe classification, significant positive trends were noted in the consumption of antibiotics from the Access (p = 0.022), Watch (p = 0.006), and Reserve (p = 0.026) categories. Conclusion. These results highlight the importance of implementing continuous antibiotic stewardship programs, as well as applying targeted interventions aimed at optimizing their use in Montenegro. Furthermore, these results contribute to global efforts in achieving a reduction in antibiotic consumption.
References
Silva AC, Nogueira PJ, Paiva JA. Determinants of antimicrobial resistance among the different European countries: more than human and animal antimicrobial consumption. Antibiotics (Basel) 2021; 10(7): 834.
Ajulo S, Awosile B. Global antimicrobial resistance and use surveillance system (GLASS 2022): Investigating the relation-ship between antimicrobial resistance and antimicrobial con-sumption data across the participating countries. PLoS One 2024; 19(2): e0297921.
Khan S, Hasan SS, Bond SE, Conway BR, Aldeyab MA. Antimi-crobial consumption in patients with COVID-19: a systematic review and meta-analysis. Expert Rev Anti Infect Ther 2022; 20(5): 749–72.
Ngoma MT, Sitali D, Mudenda S, Mukuma M, Bumbangi FN, Bunuma E, et al. Community antibiotic consumption and asso-ciated factors in Lusaka district of Zambia: findings and im-plications for antimicrobial resistance and stewardship. JAC Antimicrob Resist 2024; 6(2): dlae034.
Jiang T, Chen XS. Outcome impacts due to pathogen-specific antimicrobial resistance: A narrative review of published liter-ature. Int J Environ Res Public Health 2020; 17(4): 1395.
Goossens H, Ferech M, Vander Stichele R, Elseviers M; ESAC Project Group. Outpatient antibiotic use in Europe and associa-tion with resistance: a cross-national database study. The Lan-cet 2005; 365(9459): 579–87.
Meyer E, Gastmeier P, Deja M, Schwab F. Antibiotic consump-tion and resistance: data from Europe and Germany. Int J Med Microbiol 2013; 303(6–7): 388–95.
Pérez-Lazo G, Abarca-Salazar S, Lovón R, Rojas R, Ballena-López J, Morales-Moreno A, et al. Antibiotic consumption and its rela-tionship with bacterial resistance profiles in ESKAPE patho-gens in a Peruvian Hospital. Antibiotics (Basel) 2021; 10(10): 1221.
Barberi G, De Cola MC, Dell’Utri C, Melardi S, Alagna B, Bra-manti P, et al. Antimicrobial consumption and antimicrobial resistance: a snapshot of an Italian neuromuscular rehabilita-tion center. New Microbiol 2017; 40(2): 119–29.
Guo W, Sun F, Liu F, Cao L, Yang J, Chen Y. Antimicrobial re-sistance surveillance and prediction of Gram-negative bacteria based on antimicrobial consumption in a hospital setting: a 15-year retrospective study. Medicine (Baltimore) 2019; 98(37): e17157.
Tsutsui A, Yahara K, Shibayama K. Trends and patterns of na-tional antimicrobial consumption in Japan from 2004 to 2016. J Infect Chemother 2018; 24(6): 414–21.
Bozkurt F, Kaya S, Tekin R, Gulsun S, Deveci O, Dayan S, et al. Analysis of antimicrobial consumption and cost in a teaching hospital. J Infect Public Health 2014; 7(2): 161–9.
Klein EY, Impalli I, Poleon S, Denoel P, Cipriano M, Van Boeckel TP, et al. Global trends in antibiotic consumption during 2016–2023 and future projections through 2030. Proc Natl Acad Sci U S A 2024; 121(49): e2411919121.
Klein EY, Van Boeckel TP, Martinez EM, Pant S, Gandra S, Lev-in SA, et al. Global increase and geographic convergence in antibiotic consumption between 2000 and 2015. Proc Natl Acad Sci U S A 2018; 115(15): E3463–70.
Khouja T, Mitsantisuk K, Tadrous M, Suda KJ. Global consump-tion of antimicrobials: impact of the WHO Global Action Plan on Antimicrobial Resistance and 2019 coronavirus pan-demic (COVID-19). J Antimicrob Chemother 2022; 77(5): 1491–9.
Semenova Y, Kassym L, Kussainova A, Aimurziyeva A, Makalkina L, Avdeyev A, et al. Knowledge, Attitudes, and Practices to-wards Antibiotics, Antimicrobial Resistance, and Antibiotic Consumption in the Population of Kazakhstan. Antibiotics (Basel) 2024; 13(8): 718.
The Institute for Medicines and Medical Devices of Montenegro (CInMED). Consumption of medicines [Internet]. Montene-gro: CInMED; 2025 [cited on 2025 July 17]. Available from: https://cinmed.me/en/humane-medicines/consumption-of-medicines/ (Montenegrin)
Barnsteiner S, Baty F, Albrich WC, Babouee Flury B, Gasser M, Plüss-Suard C, et al. Antimicrobial resistance and antibiotic consumption in intensive care units, Switzerland, 2009 to 2018. Euro Surveill 2021; 26(46): 2001537.
Abu-Ajaleh S, Darwish Elhajji F, Al-Bsoul S, Abu Farha R, Al-Hammouri F, Amer A, et al. An evaluation of the impact of in-creasing the awareness of the WHO access, watch, and reserve (AWaRe) antibiotics classification on knowledge, attitudes, and hospital antibiotic prescribing practices. Antibiotics (Ba-sel) 2023; 12(6): 951.
Mudenda S, Nsofu E, Chisha P, Daka V, Chabalenge B, Mufwam-bi W, et al. Prescribing patterns of antibiotics according to the WHO AWaRe classification during the COVID-19 pandemic at a teaching hospital in Lusaka, Zambia: implications for strengthening of antimicrobial stewardship programmes. Pharmacoepidemiology 2023; 2(1): 42–53.
Sulis G, Adam P, Nafade V, Gore G, Daniels B, Daftary A, et al. Antibiotic prescription practices in primary care in low-and middle-income countries: a systematic review and meta-analysis. PLoS Med 2020; 17(6): e1003139.
Perić A, Rančić N, Dragojević-Simić V, Milenković B, Ljubenović N, Rakonjac B, et al. Association between antibiotic use and hos-pital-onset Clostridioides difficile infection in University Ter-tiary Hospital in Serbia, 2011–2021: an ecological analysis. Antibiotics (Basel) 2022; 11(9): 1178.
Sokolović D, Drakul D, Vujić‐Aleksić V, Joksimović B, Marić S, Nežić L. Antibiotic consumption and antimicrobial resistance in the SARS-CoV-2 pandemic: A single-center experience. Front Pharmacol 2023; 14: 1067973.
Sokolović D, Drakul D, Joksimović B, Lalović N, Avram N, Milić M, et al. Consumption of antibiotics in primary care setting before and during COVID-19 pandemic in Republic of Srpska, Bosnia and Herzegovina. Antibiotics (Basel) 2022; 11(10): 1319.
Duborija-Kovačević N, Djapić-Savelić J, Mijanović A. Outpatient utilization of antibacterial drugs for systemic use in Montene-gro in 2000-2022: how far are we from values and targets of the European Union? Farmacia 2025; 73(1): 140–9.
Versporten A, Bolokhovets G, Ghazaryan L, Abilova V, Pyshnik G, Spasojevic T, et al. Antibiotic use in eastern Europe: a cross-national database study in coordination with the WHO Re-gional Office for Europe. The Lancet Infect Dis 2014; 14(5): 381–7.
European Centre for Disease Prevention and Control (ECDC). An-timicrobial consumption - Annual Epidemiological Report for 2019 [Internet]. Stockholm: ECDC; 2020 [cited on 2025 July 17]. Available from: https://www.ecdc.europa.eu/en/publications-data/surveillance-antimicrobial-consumption-europe-2019
European Centre for Disease Prevention and Control (ECDC). An-timicrobial consumption in the EU/EEA (ESAC-Net) - An-nual Epidemiological Report for 2023 [Internet]. Stockholm: ECDC; 2024 [cited on 2025 July 17]. Available from: https://www.ecdc.europa.eu/en/publications-data/antimicrobial-consumption-eueea-esac-net-annual-epidemiological-report-2023
World Health Organization. WHO Regional Office for Europe Antimicrobial Medicines Consumption (AMC) Network. AMC data 2023 [Internet]. Copenhagen: WHO Regional Of-fice for Europe; 2025 [cited on 2025 July 17]. Available from: https://iris.who.int/bitstream/handle/10665/380848/9789289061872-eng.pdf?sequence=1
Wojkowska-Mach J, Godman B, Glassman A, Kurdi A, Pilc A, Rozanska A, et al. Antibiotic consumption and antimicrobial resistance in Poland; findings and implications. Antimicrob Resist Infect Control 2018; 7: 136.
Metz-Gercek S, Maieron A, Strauß R, Wieninger P, Apfalter P, Mittermayer H. Ten years of antibiotic consumption in ambula-tory care: Trends in prescribing practice and antibiotic re-sistance in Austria. BMC Infect Dis 2009; 9: 61.
The Agency for Medicinal Products and Medical Devices (HALMED). Annual report on drug utilization for 2023 – Croatian document [Internet]. Croatia: HALMED; 2023 [cit-ed on 2025 July 17]. Available from: https://www.halmed.hr/Novosti-i-edukacije/Publikacije-i-izvjesca/Izvjesca-o-potrosnji-lijekova/ (Croatian)
Medicines and Medical Devices Agency of Serbia (ALIMS). Drug sales and consumption [Internet]. Belgrade: ALIMS; 2023 [cited on 2025 July 17]. Available from: https://www.alims.gov.rs/humani-lekovi/promet-i-potrosnja-lekova/ (Serbian)
Raicevic M, Labovic Barjaktarovic S, Milic D, Nedovic Vukovic M, Bajceta N. Public knowledge, attitudes, and practices regarding antibiotics use and resistance in Montenegro. Eur J Public Health 2025; 35(2): 290–4.
Tomas A, Paut Kusturica M, Tomić Z, Horvat O, Djurović Koprivica D, Bukumirić D, et al. Self-medication with antibiotics in Ser-bian households: a case for action? Int J Clin Pharm 2017; 39(3): 507–13.
Ivanovska V, Zdravkovska M, Bosevska G, Angelovska B. Antibi-otics for upper respiratory infections: public knowledge, be-liefs and self-medication in the Republic of Macedonia. Pril (Makedon Akad Nauk Umet Odd Med Nauki) 2013; 34(2): 59–70.
Goossens H, Ferech M, Coenen S, Stephens P; European Surveillance of Antimicrobial Consumption Project Group. Comparison of out-patient systemic antibacterial use in 2004 in the United States and 27 European countries. Clin Infect Dis 2007; 44(8): 1091–5. Erratum in: Clin Infect Dis 2007; 44(9): 1259.
Gutema G, Ali S, Suleman S. Trends of community-based sys-temic antibiotic consumption: Comparative analyses of data from Ethiopia and Norway calls for public health policy ac-tions. PLoS One 2021; 16(5): e0251400.
Tshering T, Wangda S, Buising K. Trends in antimicrobial con-sumption in Bhutan. IJID Reg 2021; 1: 65–71.
Freudenhammer M, Hufnagel M, Steib-Bauert M, Mansmann U, de With K, Fellhauer M, et al. Antibiotic use in pediatric acute care hospitals: an analysis of antibiotic consumption data from Germany, 2013–2020. Infection 2024; 52(3): 825–37.
World Health Organization. The WHO AwaRe (Access, Watch, Reserve) antibiotic book [Internet]. Geneva: WHO; 2022 [cit-ed on 2025 July 17]. Available from: https://www.who.int/publications/i/item/9789240062382
Klein EY, Milkowska-Shibata M, Tseng KK, Sharland M, Gandra S, Pulcini C, et al. Assessment of WHO antibiotic consumption and access targets in 76 countries, 2000–15: an analysis of pharmaceutical sales data. Lancet Infect Dis 2021; 21(1): 107–15.
World Health Organization. WHO Regional Office for Europe Antimicrobial Medicines Consumption (AMC) Network. AMC data 2019 [Internet]. Copenhagen: WHO Regional Of-fice for Europe; 2022 [cited on 2025 July 17]. Available from: https://www.who.int/europe/publications/i/item/9789289058278
Hoxha I, Godman B, Malaj A, Meyer JC. 11-Year trend in anti-biotic consumption in a south-eastern European country; the situation in Albania and the implications for the future. Anti-biotics (Basel) 2023; 12(5): 882.