88 J Contemp Med Sci | Vol. 9, No. 2, March-April 2023: 88–92 Original The Magnitude of Dispensing Unprescribed Antibiotics in Community Pharmacies in Duhok Province; Kurdistan Region of Iraq Hind B. Almufty1*, Lara S. Hayhat2, Wasan G. Abdal3, Darya S. Hussein4, Muayad A. Merza5 1Department of Clinical Pharmacy, College of Pharmacy, University of Duhok, Kurdistan Region, Iraq. 2Department of Pharmacy, Ararat Institute, Kurdistan Region, Iraq. 3Department of Basic Science, College of Pharmacy, University of Duhok, Kurdistan Region, Iraq. 4College of Pharmacy, University of Duhok, Kurdistan Region, Iraq. 5Department of Internal Medicine, Azadi Teaching Hospital, College of Pharmacy, University of Duhok, Duhok, Kurdistan Region, Iraq. *Correspondence to: Hind B. Almufty (E-mail: Hind.bahzad@uod.ac) (Submitted: 04 February 2023 – Revised version received: 25 February 2023 – Accepted: 01 March 2023 – Published online: 26 April 2023) Abstract Objectives: The study aims to provide a descriptive overview about the magnitude and frequency of dispensing the unprescribed antibiotics UABs. It furthermore aims, to specify the most dispensed UAB types, the most common infections, signs and symptoms that require dispensing the UABs in community pharmacies of Duhok city and its districts. Methods: A cross sectional cohort study had been conducted from September to October 2022, private community pharmacies of Duhok province were included in this study. A standardized questionnaire platform was utilized to complete the survey, it included 2 sections, the first of which was related to demographic data and the second part included details of the dispensing unprescribed antibiotics UABs like: what are the most common dispensed UABs, what are the most common illness and symptoms of patients who require dispensing UABs. Results: One hundred fifty pharmacies have been included in this study. The majorities were from Duhok city 46%, and Zakho 28.7%. The prevalence of dispensing UABs was 100%, the three most common dispensed UABs were Amoxicillin 77%, followed by azithromycin 16% and cefixime 7%. The most infections and conditions requiring dispensing UABs were tonsilitis (69.3%), followed by flu and common cold (58.7%), and lower respiratory tract infection (48.7%). Conclusion: This study concluded that dispensing UABs is a frequent practice in Duhok community pharmacies. Viruses are the most common cause of upper respiratory tract infections; hence, antibiotics must be avoided and OTC medicines should be encouraged to alleviate the symptoms. Continuing medical education through training pharmacists on dispensing antibiotics by adhering to the regulations of antibiotic stewardship is crucial. Keywords: Unprescribed antibiotics, community pharmacies, infections, Kurdistan Region, Iraq ISSN 2413-0516 Introduction Antibiotic resistant crisis is the main issue that threatens global health security as it causes morbidity, mortality and magnifies the economic loss.1 In 2019, the World Health Organization (WHO) had declared that “Antimicrobial Resistance (AMR)” is one of the most urgent health risks of our time and it is named the “invisible pandemic”. Since then, serious actions had been taken worldwide to detract this scourge, i.e., using The AWaRe online tool developed by the WHO Essential Medicines List to contain rising resistances and make antibi- otics safer and more effective.2,3 Currently, it is estimated that more than 50% of antibi- otics in numerous countries are dispensed without prescrip- tions and have been utilized inappropriately such as; usage for virus treatments, wrong (broader spectrum) antibiotics used, and wrong dose and duration of treatment course, thus con- tributing to the spread of AMR.4,5 Signs of post antibiotic era had already been discovered worldwide, especially in low- and middle-income countries (LMIC).6,7 The inferior living ambience, inadequate sanitation, poor infection control, and the non-adherence to the pre- scribed course of antibiotics had been associated with AR in LMICs.8,9 However, lack of antibiotic dispensing policies in these settings and the availability of low quality of antibiotic brands are the major contributors behind this condition.10,11 Dispensing antibiotics without prescription had become a common practice in LMICs, including Iraq.11-13 Several factors contributed to this situation: the inadequate knowledge about antibiotic resistance and lack of awareness about antibiotic stewardship among community pharmacists in Iraq.13 Fur- thermore, Iraq has no community pharmacy chains meaning all community pharmacies are private independent pharma- cies usually owned by licensed pharmacists. Although, it is unwarranted by law, selling antibiotics without prescription is a common practice. On the other hand, numerous community pharmacies employ pharmacy technicians who also com- monly dispense antibiotics without prescriptions.14 To our knowledge, there is no antibiotic dispensing survey conducted in community pharmacies of Duhok province, therefore, this study aims to provide a descriptive overview about the magnitude and frequency of dispensing the UABs. It furthermore aims, to specify the most dispensed UAB types, the most common infections, signs and symptoms that require dispensing the UABs in community pharmacies of Duhok city and its districts. Materials and Methods Study Design and Setting A cross sectional cohort study had been conducted from September to October 2022 in Duhok province, Kurdistan region of Iraq. Private community pharmacies of Duhok city and its districts (Zakho, Akre, Bardaarash, Amedy, Semel and Shekhan) were studied. Governmental hospital inpatient mailto:Hind.bahzad@uod.ac 89J Contemp Med Sci | Vol. 9, No. 2, March-April 2023: 88–92 H.B. Almufty et al. Original The Magnitude of Dispensing Unprescribed Antibiotics in Community and outpatient pharmacies had been excluded as the antibi- otics are dispensed by prescription.14 Study Sampling Process A standardized questionnaire platform was utilized to complete the survey, face to face interviews were performed by the authors and the pharmacists to precisely fill the requested questions. The interviews took place in pharma- cies or any other place convenient to them. All pharmacy workers, including pharmacists and their assistants, were clearly informed about the aim of study and that the data will be kept confidential and used for research purposes only. The questionnaire included 2 sections, the first of which were questions regarding demographic data like: place, type of pharmacy (whether it is a by hand pharmacy, a medical complex pharmacy, or a private hospital phar- macy), age of the pharmacist, experience years, and the sci- entific degree of the pharmacist. The second part included details about the nature of the dispensing UABs like: what the three most common dispensed antibiotics are, what are the most common illness and symptoms of patients who require dispensing UABs, and the frequency of dispensing each type of antibiotic class were asked, whether it is com- monly dispensed (everyday), often dispensed (once to twice a week), rarely dispensed (once a month), or never dispensed. Scientific and Ethical Approval Ethical approval was obtained from the Syndicate of Kurdistan Pharmacists Duhok branch before conducting this study. This study was reviewed and approved by the scientific and Ethics Committee of the College of Pharmacy at the University of Duhok on August 7, 2022 (Reference No. 122). Written informed consent was obtained from the participants before starting the interview. Statistical Analysis All data were analyzed by Statistical Package for the Social Sciences software version 22. Descriptive statistics were car- ried out for the demographic variables, the most prevalent types of dispensed antibiotics, and to obtain the incidence of dispensing each type of antibiotic individually. Results One hundred fifty pharmacies have been included in this study. The majorities were from Duhok city 46%, followed by Duhok’s biggest district Zakho 28.7%, 4.7% were from Semel, other 14.7% included Shekhan, and Bardarash. Most of the included pharmacies were independent (by hand) ones (66%). The scientific degree of most of the interviewed pharmacists was bachelor degree (96.7%); only 5 participants had higher degrees (MSc and PhD). The mean age of the pharmacists was (28.78) ± SD 6.157, and the mean years of experience of phar- macists was (5.67) ± SD 4.874 as shown in Table 1. In the descriptive analysis, it appeared that the three most common dispensed UABs were Amoxicillin, followed by azithromycin and cefixime respectively, as shown in Figure 1. The most infections and conditions requiring dispensing UABs were tonsilitis (69.3%), followed by flu and common cold (58.7%), and lower respiratory tract infection (LRTI) (48.7%) as shown in Figure 2. Table 1. Demographic characteristics of study population Variables Number Percentage Place of pharmacy Duhok 69 46 Akre 6 4 Zakho 43 28.7 Amedy 3 2 Semel 7 4.7 Other 22 14.7 Type of pharmacy Medical complex pharmacy 39 26 Private hospital pharmacy 12 8 Independent (by hand) pharmacy 99 66 Scientific degree of the pharmacist in charge Bachelor 145 96.7 MSc 4 2.7 PhD 1 0.6 Age (mean) SD = (28.78) 6.157 Years of experience (mean) SD = (5.67) 4.874 Fig. 1 The most frequent dispensed unprescribed antibiotics. On the other hand, the most frequent signs and symp- toms that require dispensing UABs were fever, cough, sore throat, and diarrhea (68.7%, 64.7%, 51.3% and 46.7%), respec- tively (Figure 3). In this study, penicillin, macrolides, 3rd generation ceph- alosporins and quinolones were among the most common dis- pensed antibiotics. Fourth and 5th generation cephalosporins, linconsamide, streptogramine, linezolid, daptomycin, lefam- ulin, monobactam, fosfomycin, nitrofurantoin, sulphonamids, and chloramphenicol were the antibiotic classes that fall among those which rarely to never dispensed without a pre- scription (Table 2). Discussion The antibiotic resistance continuously spreads worldwide, particularly in LMIC, including Iraq. There is an urgent need 90 J Contemp Med Sci | Vol. 9, No. 2, March-April 2023: 88–92 The Magnitude of Dispensing Unprescribed Antibiotics in Community Original H.B. Almufty et al. Fig. 2 The most frequent conditions that require dispensing unprescribed antibiotics. Fig. 3 The most common signs and symptoms that require dispensing unprescribed antibiotics. to set an antibiotic dispensing policy and improve prescription practices through incorporating treatment recommendations into the national guidelines, and consolidation of the aware- ness of this public health problem.15 In our study, the dispensing of UABs was high, which is in line to studies from Syria, Egypt, and Saudi Arabia.16,17 How- ever, studies from Qatar and other high-income countries like, North America, Europe, and Australia showed a low preva- lence of dispensing UABs.11,18-20 The irresponsible malpractice of frequent UAB uses in Duhok community pharmacies is threatening the community health security outcome in the region. Moreover, the high prevalence (93.7%) of antibiotic misuse in Kurdistan hospitals perplexed the emergence of antibiotic resistance.21 Therefore, it is crucial to encourage dis- pensing prescribed antibiotics and to avoid dispensing UABs by pressing charges through the pharmacy council against the pharmacist who do not adhere to rational uses of antibiotics. In our study, we found that the most frequent dispensed UABs in the private health sector were amoxicillin with or without clavulanic acid, followed by azithromycin, and cefixime. The prevalent use of unprescribed amoxicillin has been well documented in several LMICs countries.22-24 In Iraq, the wrong belief of using specific antibiotics such as amoxi- cillin and azithromycin for treating respiratory tract infections including viral in origin is a challenging consequence of increasing antibiotic resistance. The increase of such antibiotic consumptions in winter is well recognized14 It is worthy to mention that the use of azithromycin has increased dramati- cally after COVID-19 pandemic, particularly in the early phase of the pandemic as it was used in the treatment guide- line of COVD-19 patients.25,26 This finding rationalizes the extreme pathogen resistance to these antibiotics in the region.27-29 While other studies from the same region showed a high rate of inappropriate 3rd generation cephalosporin 91J Contemp Med Sci | Vol. 9, No. 2, March-April 2023: 88–92 H.B. Almufty et al. Original The Magnitude of Dispensing Unprescribed Antibiotics in Community Table 2. The frequency of dispensing antibiotics in community pharmacies The antibiotics The dispensing (%) Commonly Often Rarely Never Sulphonamides 1.3 10 24.7 64 Penicillin 94 6 – – 1st generation cephalosporin 16 35.3 22 26.7 2nd generation cephalosporin 5.4 15.3 17.3 62 3rd generation cephalosporin 46 32.7 9.3 12 4th generation cephalosporin – – 6.7 93.3 5th generation cephalosporin – – – 100 carbapenem 1.3 2 12 84 Glycopeptide – – 7.3 92.7 Monobactam – – 2 98 Aminoglycosides 7.3 20.7 28 44 Macrolides 66 30 2.7 1.3 Chloramphenicol 1.3 9.3 11.3 78 Quinolone 33.3 36.7 16 14 Fosfomycin, nitrofurantoin 0.7 2 17.3 80 Linconsamide 1.3 5.3 6 87.3 Streptogramine – – 0.7 99.3 Linezolid – – – 100 Daptomycin – – – 100 Lefamulin – – – 100 prescriptions in the governmental sector,21 which increases the magnitude of AMR in our region. Overall, continuing medical education through training of pharmacists on antibiotics dis- pensation by adhering to the regulations of antibiotic steward- ship is crucial. In the present study, the unprescribed quinolones, in par- ticular ciprofloxacin was used often (2–3 times a week); whereas, other studies reported metronidazole and quinolones as most frequent dispensed UAB.24,30,31 It is noteworthy that 80% and 44% of Duhok community pharmacies never dis- pense unprescribed nitrofurantoin and aminoglycoside class, respectively, that elucidates to the lowest rate of resistance of these antibiotics for treating urinary tract infection (UTI).32 The higher rate of broad-spectrum antibiotic such as cipro- floxacin for treating UTI, instead of narrow-spectrum antibi- otic such as nitrofurantoin, is malpractice in enhancing AMR. Therefore, clinical pharmacists should play a pivotal role in avoiding the use of broad-spectrum antibiotics, consequently encouraging the use of narrow-spectrum antibiotics for spe- cific infections. In the current study, UABs were dispensed for the treat- ment of tonsilitis (23.4%), flu and common cold (19.8%), and other upper respiratory tract infection (URTI) (16.4%). This finding was concordant with a study from China where URTIs were the most frequent reason for UABs.11 On the contrary, a study from Nigeria reported that UTIs, typhoid fever, and sex- ually transmitted diseases (STD) were the most infections that require dispensing UABs.33 While in Saudi Arabia, pharma- cists dispense UABs for pharyngitis and UTI most commonly34 In general, the differences of dispensing UABs between different countries is guided by local epidemiology infections. Concerning high rates of antibiotic misuse for URTIs, com- munity pharmacists should be involved actively in avoiding dispensing UABs by offering over the counter (OTC) medi- cines that alleviate upper respiratory symptoms of viral origin such as painkillers for fever and aches, and antihistamines for sneezing and an itchy nose. The main limitation of the study was the slight possibility of having imprecise data, as this method “pharmacy inter- views” may be exposed to the Hawthorne effect (changes in the behavior of the studied pharmacists because they feel observed).15 Another limitation was that our study was con- fined to one province. Hence, we recommend larger studies at national level to better understand the magnitude of UBA dispensations. Conclusion This study concluded that dispensing UABs is a frequent prac- tice in Duhok community pharmacies. Amoxicillin, azithro- mycin, and cefixime are the most widely dispensed antibiotics. Tonsilitis, flu and common cold, and other URTI are the con- ditions requiring the most dispensations of UABs; while fever, cough and sore throat are the most reported signs and symp- toms for UAB dispensations. Viruses are the most common cause of URTIs, hence, antibiotics must be avoided and OTC medicines should be encouraged to alleviate the symptoms. Continuing medical education through training pharmacists on dispensing antibiotics by adhering to the regulations of antibiotic stewardship is crucial. 92 J Contemp Med Sci | Vol. 9, No. 2, March-April 2023: 88–92 The Magnitude of Dispensing Unprescribed Antibiotics in Community Original H.B. Almufty et al. Acknowledgments The authors would like to thank all community pharmacies in Duhok for their cooperation and contribution, their efforts are highly appreciated. Conflict of Interest The authors declare no conflict of interest. Financial Support N.A. Data Availability Statement The data that support the findings of this study are avail- able from the corresponding author upon reasonable request.  References 1. Organization WH. Antimicrobial resistance global report on surveillance: 2014 summary. World Health Organization; 2014. 2. UN health agency steps up fight against ‘invisible pandemic’ of antimicrobial resistance [Internet]. 2019. Available from: https://news. un.org/en/story/2019/06/1040741. 3. Organization WH. In the face of slow progress, WHO offers a new tool and sets a target to accelerate action against antimicrobial resistance. 2019. 4. Grigoryan L, Haaijer-Ruskamp FM, Burgerhof JG, Mechtler R, Deschepper R, Tambic-Andrasevic A, et al. Self-medication with antimicrobial drugs in Europe. Emerging infectious diseases. 2006;12(3):452. 5. Cars O, Nordberg P. Antibiotic resistance–The faceless threat. International Journal of Risk & Safety in Medicine. 2005;17(3-4):103–10. 6. Laxminarayan R, Matsoso P, Pant S, Brower C, Røttingen J-A, Klugman K, et al. Access to effective antimicrobials: a worldwide challenge. The Lancet. 2016;387(10014):168–75. 7. Rambliere L, Guillemot D, Delarocque-Astagneau E, Huynh B-T. Impact of mass and systematic antibiotic administration on antibiotic resistance in low-and middle-income countries. A systematic review. International Journal of Antimicrobial Agents. 2021;58(1):106364. 8. Ayukekbong JA, Ntemgwa M, Atabe AN. The threat of antimicrobial resistance in developing countries: causes and control strategies. Antimicrobial Resistance & Infection Control. 2017;6(1):1–8. 9. Hadi U, Duerink DO, Lestari ES, Nagelkerke NJ, Werter S, Keuter M, et al. Survey of antibiotic use of individuals visiting public healthcare facilities in Indonesia. International Journal of Infectious Diseases. 2008;12(6):622–9. 10. Morgan DJ, Okeke IN, Laxminarayan R, Perencevich EN, Weisenberg S. Non- prescription antimicrobial use worldwide: a systematic review. The Lancet Infectious Diseases. 2011;11(9):692–701. 11. Chang J, Xu S, Zhu S, Li Z, Yu J, Zhang Y, et al. Assessment of non- prescription antibiotic dispensing at community pharmacies in China with simulated clients: a mixed cross-sectional and longitudinal study. The Lancet Infectious Diseases. 2019;19(12):1345–54. 12. Al-Halawa DA, Sarama R, Abdeen Z, Qasrawi R. Knowledge, attitudes, and practices relating to antibiotic resistance among pharmacists: a cross- sectional study in the West Bank, Palestine. The Lancet. 2019;393:S7. 13. Alkadhimi A, Dawood OT, Hassali MA. Dispensing of antibiotics in community pharmacy in Iraq: a qualitative study. Pharmacy Practice (Granada). 2020;18(4). 14. Al-Jumaili AA, Hussein AH, Al-Rekabi MD, Raheem SA, Ernst EJ. Antimicrobial utilization in an Iraqi province: a comprehensive evaluation of antibiotic source and cost. International Journal of Pharmacy Practice. 2017;25(1):81–8. 15. Batista AD, A. Rodrigues D, Figueiras A, Zapata-Cachafeiro M, Roque F, Herdeiro MT. Antibiotic dispensation without a prescription worldwide: a systematic review. Antibiotics. 2020;9(11):786. 16. Mahmoud MA, Aldhaeefi M, Sheikh A, Aljadhey H. Community pharmacists’ perspectives about reasons behind antibiotics dispensing without prescription: a qualitative study. Biomedical Research. 2018;29(21):3792–6. 17. Mansour O, Al-Kayali R. Community pharmacists’ role in controlling bacterial antibiotic resistance in Aleppo, Syria. Iranian Journal of Pharmaceutical Research: IJPR. 2017;16(4):1612. 18. Mohamed Ibrahim MI, Awaisu A, Palaian S, Radoui A, Atwa H. Do community pharmacists in Qatar manage acute respiratory conditions rationally? A simulated client study. Journal of Pharmaceutical Health Services Research. 2018;9(1):33–9. 19. Zapata-Cachafeiro M, Piñeiro-Lamas M, Guinovart MC, López-Vázquez P, Vázquez-Lago JM, Figueiras A. Magnitude and determinants of antibiotic dispensing without prescription in Spain: a simulated patient study. Journal of Antimicrobial Chemotherapy. 2019;74(2):511–4. 20. Khan MU, Hassali MAA, Ahmad A, Elkalmi RM, Zaidi STR, Dhingra S. Perceptions and practices of community pharmacists towards antimicrobial stewardship in the state of Selangor, Malaysia. PloS One. 2016;11(2):e0149623. 21. Kurdi A, Hasan AJ, Baker KI, Seaton RA, Ramzi ZS, Sneddon J, et al. A multicentre point prevalence survey of hospital antibiotic prescribing and quality indices in the Kurdistan Regional Government of Northern Iraq: The need for urgent action. Expert Review of Anti-infective Therapy. 2021;19(6):805–14. 22. Al-Mohamadi A, Badr A, Mahfouz LB, Samargandi D, Al Ahdal A. Dispensing medications without prescription at Saudi community pharmacy: extent and perception. Saudi Pharmaceutical Journal. 2013;21(1):13–8. 23. Kalungia AC, Burger J, Godman B, Costa JdO, Simuwelu C. Non-prescription sale and dispensing of antibiotics in community pharmacies in Zambia. Expert Review of Anti-infective Therapy. 2016;14(12):1215–23. 24. Damisie G, Hambisa S, Yimam M. Over the counter sale of antibiotics at drug stores found in Mizan-Aman Town, Southwest Ethiopia: a cross-sectional simulated client visit study. Journal of Pharmaceutics. 2019;2019. 25. Cavalcanti AB, Zampieri FG, Rosa RG, Azevedo LC, Veiga VC, Avezum A, et al. Hydroxychloroquine with or without azithromycin in mild-to-moderate Covid-19. New England Journal of Medicine. 2020;383(21):2041–52. 26. Merza MA, Al Mezori AAH, Mohammed HM, Abdulah DM. COVID-19 outbreak in Iraqi Kurdistan: The first report characterizing epidemiological, clinical, laboratory, and radiological findings of the disease. Diabetes & Metabolic Syndrome: Clinical Research & Reviews. 2020;14(4):547–54. 27. Hussein NR, Daniel S, Salim K, Assafi MS. Urinary tract infections and antibiotic sensitivity patterns among women referred to Azadi teaching hospital, Duhok, Iraq. Avicenna Journal of Clinical Microbiology and Infection. 2017;5(2):27–30. 28. Hasan TH, Alasedi KK, Aljanaby AAJ. A Comparative Study of Prevalence Antimicrobials Resistance Klebsiella pneumoniae among Different Pathogenic Bacteria Isolated from Patients with Urinary Tract Infection in Al-Najaf City, Iraq. Latin American Journal of Pharmacy. 2021;40:174–8. 29. Hasan SA, Najati AM, Abass KS. Prevalence and antibiotic resistance of “pseudomonas aeruginosa” isolated from clinical samples in Kirkuk City, Iraq. Eurasia J Biosci. 2020;14(1):1821–5. 30. Ibrahim IR, Palaian S, Ibrahim MI. Assessment of diarrhea treatment and counseling in community pharmacies in Baghdad, Iraq: A simulated patient study. Pharmacy Practice (Granada). 2018;16(4). 31. Zawahir S, Lekamwasam S, Aslani P. Antibiotic dispensing practice in community pharmacies: A simulated client study. Research in Social and Administrative Pharmacy. 2019;15(5):584–90. 32. Abdullah IM. Multiple drugs resistance among urinary tract infection patients in Duhok city–Kurdistan Region–Iraq. Duhok Medical Journal. 2019;13(1):22–31. 33. Abubakar U, Tangiisuran B. Knowledge and practices of community pharmacists towards non-prescription dispensing of antibiotics in Northern Nigeria. International Journal of Clinical Pharmacy. 2020;42(2):756–64. 34. Alrasheedy AA, Alsalloum MA, Almuqbil FA, Almuzaini MA, Aba Alkhayl BS, Albishri AS, et al. The impact of law enforcement on dispensing antibiotics without prescription: a multi-methods study from Saudi Arabia. Expert Review of Anti-infective Therapy. 2020;18(1):87–97. This work is licensed under a Creative Commons Attribution-NonCommercial 3.0 Unported License which allows users to read, copy, distribute and make derivative works for non-commercial purposes from the material, as long as the author of the original work is cited properly. https://doi.org/10.22317/jcms.v9i2.1324 https://news.un.org/en/story/2019/06/1040741 https://news.un.org/en/story/2019/06/1040741