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Knowledge, attitudes and behaviour of Egyptians towards antibiotic use in the community: can we do better?

Knowledge, attitudes and behaviour of Egyptians towards antibiotic use in the community: can we... Background Infectious diseases are among the leading causes of death worldwide. This is concerning because of the increasing capacity of the pathogens to develop antibiotic resistance. Antibiotic overuse and misuse remain the main drivers of resistance development. In the USA and Europe, annual campaigns raise awareness of antibiotic misuse hazards and promote their judicial use. Similar efforts are lacking in Egypt. This study assessed the knowledge of the public in Alexandria, Egypt of antibiotic misuse risks and their habits towards antibiotic use, in addition to conducting a campaign to increase awareness of the safe use of antibiotics. Methods A questionnaire assessing knowledge, attitudes and behaviour towards antibiotics was used to collect responses from study participants at various sports clubs in Alexandria in 2019. An awareness campaign to correct misconceptions and a post awareness survey followed. Results Most of the participants were well-educated (85%), in their middle age (51%) and took antibiotics last year (80%). 22% would take an antibiotic for common cold. This dropped to 7% following the awareness. There was a 1.6 time increase in participants who would start an antibiotic on a healthcare professional’s advice following the campaign. A 1.3 time increase in participants who would finish an antibiotic regimen was also observed. The campaign made all participants recognize that unwise antibiotic use is harmful to them or others; and 1.5 more participants would spread the word about antibiotic resistance. Despite learning of the risks of antibiotic use, there was no change in how often participants thought they should take antibiotics. Conclusions Although awareness of antibiotic resistance is rising, some wrong perceptions hold fast. This highlights the need for patient and healthcare-tailored awareness sessions as part of a structured and national public health program directed to the Egyptian population. Keywords Antibiotic resistance, Awareness campaign, Educational intervention, Common cold, The theory of planned behaviour *Correspondence: Department of Pharmacy Practice and Clinical Pharmacy, Faculty of Alaa Abouelfetouh Pharmacy, Alamein International University, New Alamein City alaa.abouelfetouh@pharmacy.alexu.edu.eg 51718, Egypt 1 4 Department of Microbiology and Immunology, Faculty of Pharmacy, Department of Microbiology and Immunology, Faculty of Pharmacy, Alexandria University, 1 Khartoum Sq, Azarita, Alexandria 21521, Egypt Alamein International University, New Alamein City 51718, Egypt Norwich Medical School, University of East Anglia, Norwich, UK © The Author(s) 2023. 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The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Maarouf et al. Antimicrobial Resistance & Infection Control (2023) 12:50 Page 2 of 9 Background Kholy et al. found that around 70% of Staphylococcus Antimicrobial resistance (AMR) represents a serious aureus isolates were resistant to a wide range of antibi- problem described by the World Health Organization otic classes. Another study reported fluoroquinolone (WHO) as “a global public health concern” [1]. AMR resistance among methicillin-resistant S. aureus (MRSA) has dire consequences worldwide as it increases mor- isolates from Alexandria, Egypt to range between 78% bidity and mortality rates from bacterial infection and and 96% [16]. Among Gram negative pathogens, 94% mandates quick interventions to mitigate the problem of E. coli isolates were resistant to ampicillin [17] and [2]. In the last three decades, the rate of approval of new upward of 70% of Acinetobacter baumannii isolates from antibiotics has slowed while antibiotic resistant bacte- Alexandria Main University Hospital were MDR [18]. rial pathogens have continued to emerge [3]. Moreover, However, only a small number of studies reported the pathogens keep acquiring more resistance determinants percentage of antibiotic misuse among Egyptian com- leading to the emergence of multidrug-resistant (MDR) munity pharmacies. Abdelaziz et al. reported that 98% of and even extensive drug-resistant (XDR) and pan drug- the visited pharmacies dispensed an antibiotic as an over resistant (PDR) bacteria which are resistant to all antibi- the counter (OTC) drug to treat ‘flu symptoms’ [ 19]. In otics [4]. another report, Dooling et al. mentioned that 64% and The emergence of these resistant bacteria leads to 81% of participating physicians and pharmacists, respec- a socioeconomic burden worldwide due to increased tively, from Minya, Egypt were prescribing antibiotics for healthcare costs as a result of using more expensive anti- patients with symptoms consistent with a common cold microbials and prolonged hospital stays, in addition to [20]. Moreover, a “cold group” that is a combination of lost productivity. It is estimated that the annual health pills, that may contain antibiotics, and that is commonly burden of the treatment of MDR bacterial infections in sold in some Egyptian pharmacies to treat common cold the USA is around $20 billion, with $35 billion lost due to was provided to simulated clients in 28.7% of the cases. reduced productivity [3], and a global annual death toll of In all of these, the cold group contained one or more 700,000 in 2014 that is expected to increase to 10 million antibiotic pills [21]. by 2050 [5]. Patient pressure has been identified as an important Research from around the globe indicates high rates driver for injudicious prescribing and dispensing of anti- of injudicious use of antibiotics by the public. Practices biotics, yet a lone campaign in Minya, Egypt promoted related to injudicious use in the literature include the use the appropriate use of antibiotics to treat respiratory tract of left over antibiotics [6, 7] and antibiotic non-adherence infections among prescribers and the general public [22]. usually due to remission of symptoms [8]. Further, the The aim of the current work was to assess the knowledge pressure made by patients who request antibiotics from of antibiotic resistance among the public in Alexandria, clinicians has been shown to be one of the factors driving Egypt and their attitudes towards antibiotic use. More- unwarranted provision of antibiotics by clinicians such over, an awareness campaign was designed to educate the as physicians [9] and pharmacists [10]. Antibiotic abuse participants on appropriate antibiotic use principles. The and misuse in the form of overuse or underuse remain knowledge was re-assessed at the conclusion of the cam- some of the most important factors contributing to paign to measure its effectiveness. In order to achieve resistance development particularly in developing coun- these aims we targeted the parents of children attending tries (reviewed in [11]). A study investigating the driv- sports clubs, as this would allow us to repeatedly inter- ers of antibiotic use and misuse in the community found act with the same individuals over the course of several patient behaviour to be an important driving factor. This weeks. To the best of the authors’ knowledge, this is the takes the form of patients putting pressure on a physician second published awareness campaign in Egypt and the to prescribe an unnecessary antibiotic either directly by first in Alexandria to address wise antibiotic use among demanding an antibiotic or indirectly when questioning the general public. the absence of an antibiotic in a prescription [12, 13]. Moreover, many patients believe they have the right to Methods self-prescribe an antibiotic or get one from friends and A questionnaire was used to collect responses from study family [14]. About 50% of antibiotic use is done improp- participants who were the parents of children playing erly in the form of using the wrong agent or the wrong sports at different sports clubs in Alexandria, Egypt. The dose or duration (reviewed in [11]). study was conducted over three months between July and In Egypt, antibiotic misuse and overuse led to a high September 2019. It was divided into three phases. Phase prevalence of MDR bacteria among the population one consisted of a general survey about participant’s anti- (reviewed in [15]). Most studies comment on the resis- biotic use and knowledge of antibiotic resistance. Phase tance rates among a particular MDR pathogen rather two consisted of an antibiotic awareness campaign to than on the general prevalence of MDR organisms. El guide people against the misuse of antibiotics and its Maarouf et al. Antimicrobial Resistance & Infection Control (2023) 12:50 Page 3 of 9 consequences on antibiotic resistance, and phase three Data analysis consisted of a post awareness questionnaire to assess the The data were tabulated and statistically analysed using effectiveness of the awareness sessions. The awareness Fisher’s exact test and Chi squared test, where the results sessions were delivered by Alexandria University clinical were considered significant at a p value of ≤ 0.05. The pharmacy students and took the form of informal chats Independent variable was the education, and the depen- with the participants. As part of the sessions, the partici- dent variables were knowledge and attitudes towards pants were given some flyers (Additional File 1) stressing antibiotic use and resistance. Categorical variable was the awareness messages. The students took turns deliver - classified to Zero (unexposed to education), 1 (exposed ing the messages and used the flyers as guiding points. to education). Data showing significant differences were Ethical approval for the study was obtained from the subsequently analysed by binary or multinomial logistic Faculty of Medicine and Health Sciences Research Eth- regression in SPSS (v. 28.0.1.1) to obtain odds ratios. For ics Committee, University of East Anglia (Reference multinomial regression, the reference category was set as 201,819–102), and The Research Ethics Committee at the the largest category for each dataset. Faculty of Pharmacy, Alexandria University prior to study commencement. Results A total of 626 sports club attendees were approached Sampling and they all agreed to participate in the study making Convenience sampling was used to recruit the partici- the response rate 100%. The majority of the participants pants. No specific sample size was designated before (51%) were aged 31 to 50 years old, 76% of the partici- study commencement. The sample size was determined pants were females and 85% were university graduates in light of the number of students contributing to the holding a bachelor or a higher degree. campaign. The students set up working stations on week - Surveying the history of antibiotic use showed that days and weekends in each of the sports clubs they vis- more than 80% of the participants took antibiotics last ited and approached all adults who came in contact with year at least once, with 46% taking antibiotics 2 to 3 them. All potential study participants were provided with times. Of those who had taken antibiotics, 80% took them a participant information sheet prior to taking part in the on the advice of a healthcare professional (62% from a study, and informed consent was obtained from all par- doctor, 18% from a pharmacist), while 20% took them ticipants for the collection and use of their data before after advice from non-healthcare professional sources beginning the study. The participants were then given the (13% decided themselves, 6% from a family member, 1% paper-based questionnaire by the students. The partici - from a friend) (Table  1). On the other hand, more than pants returned the completed questionnaire back to the 50% of the participants said that they were informed by students when they were done. their physician that they don’t need an antibiotic to treat their symptoms, yet > 80% of the participants took antibi- Design of the questionnaire otics in the previous year. The questionnaire (Additional File 2 shows the Arabic Looking at participant knowledge of antibiotic use, 35% version and Additional File 3 shows the English transla- of the participants believed that more expensive antibiot- tion) covered the demographic and professional data of ics would be more effective. This percentage was almost the participants and then was divided into two parts. The halved following the campaign (binary logistic regression, first part consisted of six questions collecting data about OR = 0.431, 95% CI = 0.196–0.945, p = 0.036). A total of past antibiotic use. The second part contained 13 ques - 78% of the participants thought that they should not take tions about knowledge and attitudes towards antibiotics antibiotics for a common cold; this percentage increased and antibiotic resistance. The participants were asked to 93% after the campaign (binary logistic regression, to fill both parts of the questionnaire at phase one, and OR = 0.255, 95% CI = 0.078–0.837, p = 0.024). Yet, almost just the second part at phase three following the aware- half of the participants would start an antibiotic based on ness campaign. The full questionnaire needed an average their own assessment of their symptoms versus 34% who of five minutes to be completed. A pilot study covering would start an antibiotic following advice from a physi- over 500 participants had been carried out prior to cur- cian or pharmacist. These percentages changed to 20% rent data collection. and 55% following the awareness campaign (Chi squared The questionnaire was anonymous, the demographic test, p < 0.001). Nevertheless, 64% of the participants data collected can’t be used to determine the identity of knew that they should complete the antibiotic regimen, the participants, and therefore the data from phase one which increased to 86% as a consequence of the aware- and phase three can’t be linked to individuals. ness campaign (Chi squared test, p < 0.001) (Table 2). Concerning participants’ attitudes towards antibiotic use, only 18% reported that they would put pressure on Maarouf et al. Antimicrobial Resistance & Infection Control (2023) 12:50 Page 4 of 9 Table 1 Participant demographics and antibiotic use in the test, p < 0.001). As for participant’ attitudes towards anti- previous year biotic resistance, 87% have now told others about anti- Number Percentage biotic resistance versus just 59% before the campaign Age group (years) 192 30.7 (binary logistic regression, OR = 4.729, 95% CI = 1.818– 18–30 320 51.1 12.301, p = 0. 001), yet the campaign does not seem to 31–50 92 14.7 have changed how often people would take an antibiotic 51–70 22 3.5 > 70 (Table 3). Gender 478 76.4 Female 146 23.3 Discussion Male 2 0.3 Antibiotic resistance, which is a worldwide crisis, is a Prefer not to say crucial problem; and urgent action is needed to resolve Level of education 95 15.2 it. One of the important pillars in combatting AMR is Postgraduate 435 69.5 improving public knowledge of antibiotic use [23]. Glob- Bachelor 85 13.6 High school graduate 10 1.6 ally, many antibiotic awareness campaigns have been Middle school graduate 1 0.2 conducted to increase public understanding of the risks None around the misuse of antibiotics and the threat from Antibiotic use in last year 184 35.5 antibiotic resistance. For instance, European Antibiotic Once 241 46.4 Awareness Day (EAAD), which was launched in 2008 is 2–3 times 94 18.1 an annual event co-ordinating public engagement activi- ≥ 4 times Who advised you to take the antibiotics? 345 62.4 ties across Europe [24], and World Antibiotic Awareness Doctor 99 17.9 Week, which was firstly introduced by WHO in 2015, is Pharmacist 0 0 held in the middle of November annually [25]. Therefore, Nurse 6 1.1 this study aimed to assess public knowledge and then Friend 31 5.6 determine the impact of an awareness campaign designed Family member 70 12.7 Self 2 0.4 to provide the public with information about appropriate Other antibiotic use and the problem of resistance. Promising findings from this study are in line with recent research the physician to prescribe an antibiotic, which dropped in Egypt showing an improvement in prescribing habits, to 7% after the campaign (Fisher’s exact test, p = 0.031; attitude and belief scores for physicians, pharmacists, and binary logistic regression, OR = 0.353, 95% CI = 0.107– patients regarding antibiotic use following a campaign in 1.162, p = 0.087). While there was also a significant drop Minya, a governorate in Southern Egypt [22]. in the number of participants who would buy antibiotics Although the sample size was not pre-determined and to use even if a doctor hadn’t told them they needed them it mainly depended on the number of students deliver- (34% before the awareness campaign vs. 17% after; binary ing the survey and awareness campaign, given the large logistic regression, OR = 0.409, 95% CI = 0.178–0.938, number of participants in the study and the significance p = 0.035), there remained a substantial number of peo- of findings we do not anticipate that inadequate power ple who would still purchase antibiotics. This was further was to be an issue of concern. In general, most of the reflected in the fact that there was no significant differ - tested population (85%) used antibiotics throughout ence in the number of participants who felt they should the last year, which is almost the same percentage (89%) be able to buy antibiotics whenever they want them, with described in a recent WHO report [26] that studied anti- almost one in three participants wanting the freedom to biotic use in different countries including Egypt. 80% do so (Table 2). of the participants had been prescribed antibiotics by Regarding antibiotic resistance, 78% of participants healthcare professionals, and only 13% were self-medi- had already heard about the problem even before the cated; this percentage is lower than previously reported campaign; this occurred through interaction with a by WHO (26%) [26] and in an Egyptian study on non- healthcare practitioner in 47% of cases and through the medical students (39%) [27]. This could be explained by media in 33% (Table 3). It is of note that as many people the high percentage of well-educated participants in our had heard about antibiotic resistance from a physician study who also tend to be wealthier. As such, they could or a nurse as had heard about it from the media (33% in afford to consult with healthcare professionals rather both cases). Despite hearing about antibiotic resistance, than being forced to self-medicate. about 11% thought that unwise antibiotic use won’t have Moreover, one third of participants believed that the a harmful effect. Following the awareness campaign, more expensive an antibiotic is, the more effective it is. 100% of the participants appreciated that resistance is a This could be explained by the perception in general that problem for everyone now and in the future (Chi squared any product with a higher price will be higher in quality, Maarouf et al. Antimicrobial Resistance & Infection Control (2023) 12:50 Page 5 of 9 Table 2 Participant knowledge and attitudes towards antibiotics before and after the awareness sessions Participant knowledge Before After p value Regression awareness awareness n % n % p value Odds Lower Upper ratio 95% 95% CI CI Do you believe more expensive antibiotics are more 216 34.7 8 18.6 0.011455 0.036 0.431 0.196 0.945 likely to make you feel better? 407 65.3 35 81.4 Yes No Do you believe you have to take an antibiotic when- 139 22.3 3 7 0.004288 0.024 0.255 0.078 0.837 ever you have an infection, like a cold? 483 77.7 40 93 Yes No When you get a cold, when do you think you should 88 14.1 11 25 2.67021E-07 0.845 1.078 0.506 2.296 start taking antibiotics? 71 11.4 3 6.8 0.108 0.364 0.107 1.247 I don’t take them 124 19.9 4 9.1 0.02 0.278 0.094 0.821 When feeling the first symptoms of a cold 105 16.8 2 4.5 0.015 0.164 0.038 0.708 After cough and sputum appear 207 33.2 24 54.5 Ref - - - After the colour of mucous changes 1 0.2 0 0 - - - - After a doctor or pharmacist tells me to take one 18 2.9 0 0 - - - - I have never had a cold 10 1.6 0 0 - - - - I don’t know Others When you have been taking antibiotics, when do 202 32.5 5 11.6 6.41626E-05 0.006 0.266 0.103 0.686 you think you should stop the antibiotic treatment? 397 63.8 37 86 Ref - - - When I feel better 18 2.9 1 2.3 0.619 0.596 0.077 4.592 After I finish the full course 5 0.8 0 0 - - - - I have never taken antibiotics I don’t know Participant attitudes Before After p value  Regression awareness awareness n % n % p value  Odds  Lower Upper ratio 95% 95% CI CI  Would you ask a doctor to prescribe an antibiotic if 109 17.5 3 7 0.030886 0.087 0.353 0.107 1.162 you believe you need one, even if the doctor did not 513 82.5 40 93 think it was needed? Yes No Would you buy antibiotics to use without being told 208 33.5 7 17.1 0.013828 0.035 0.409 0.178 0.938 you need them by a doctor? 413 66.5 34 82.9 Yes No Do you think you should be able to buy antibiotics 188 30.3 11 26.8 0.642698 nd nd nd nd whenever you want them? 433 69.7 30 73.2 Yes No Ref indicates this is the reference category in multinomial logistic regression analyses. nd, not done as initial analysis reported no significant difference. Dashes (-) in p value, OR and 95% CI columns for multinomial regression represent non-returned values due to insufficient data. Answers to some questions were missing neglecting its actual properties [28]. However, as a result misconception, with only 7% of people saying they would of the campaign, this percentage was almost halved. take an antibiotic for a cold after taking part. Similarly, In total 22% of the participants believed that antibiotics concerning the completion of the antibiotic course, 64% could be used to treat the common cold, which is much of participants believed that they should complete their lower than found in the WHO’s report (76%) [26] and antibiotic course, which is high compared to the WHO close to what was published in a survey in 2017 in Eng- report (41%) [26]. However, this value increased to 86% land (15%) [29]. In these studies, the participants may not after the campaign, which comes near the rate described have been aware that the common cold is a viral infection in the English report (87%) [29]. The high level of aware - that could not be treated by antibiotics. Our awareness ness of the need to complete the antibiotic course seen campaign was particularly effective at correcting this Maarouf et al. Antimicrobial Resistance & Infection Control (2023) 12:50 Page 6 of 9 Table 3 Participant knowledge and attitudes towards antibiotic resistance before and after the awareness sessions Participant knowledge Before After p value Regression awareness awareness n % n % p value Odds Lower Upper ratio 95% 95% CI CI How many times have you heard about antibiotic 388 62.9 30 69.8 8.97963E-13 Ref - - - resistance? 43 7 0 0 - - - - Many times 50 8.1 11 25.6 0.006 2.845 1.343 6.03 A few times 136 22 2 4.7 0.024 0.19 0.045 0.806 Only once I don’t remember hearing about antibiotic resistance Where have you heard about antibiotic resistance? 167 33.2 6 15 3.41269E-32 0.594 0.746 0.253 2.195 From a physician or nurse 69 13.7 19 47.5 0.00009 5.714 2.388 13.672 From a pharmacist 70 13.9 5 12.5 0.503 1.482 0.468 4.689 From friends or family 29 5.8 0 0 - - - - At school/college/university 166 33 8 20 Ref - - - In the media (television, radio, newspapers, magazines 2 0.4 2 5 0.004 20.75 2.581 166.828 etc.) Others How widespread do you think antibiotic resistance is? 52 11 4 10.3 0.110692 nd nd nd nd Mostly found in rich countries 153 32.3 9 23.1 Mostly found in poor countries 269 56.8 26 66.7 Worldwide What do you think will happen if you use antibiotics 54 11 0 0 0.000175 - - - - unnecessarily? 211 42.9 18 46.2 Ref - - - Nothing 24 4.9 0 0 - - - - Antibiotic-resistant infections will personally affect me 203 41.3 21 53.8 0.566 1.213 0.628 2.342 Antibiotic-resistant infections will affect others in the future Antibiotic-resistant infections will affect me, and others in the future Participant attitudes Before After p value  Regression awareness awareness n % n % p value Odds  Lower Upper ratio  95% 95% CI CI  Has hearing about antibiotic resistance changed how 36 7.6 3 8.1 0.46244164 nd nd nd nd often you think you should take antibiotics? 352 74.1 29 78.4 Yes – I think I should take them more 87 18.3 5 13.5 Yes – I think I should take them less No Have you told anyone else about antibiotic resistance? 289 59 34 87.2 7.4E-06 0.001 4.729 1.818 12.301 Yes 201 41 5 12.8 No Ref indicates this is the reference category in multinomial logistic regression analyses. nd, not done as initial analysis reported no significant difference. Dashes (-) in p value, OR and 95% CI columns for multinomial regression represent non-returned values due to insufficient data. Answers to some questions were missing in the current study might be explained by the high per- participants thought that there will be no harmful effects centage of well-educated participants. from antibiotic resistance in the future, this concept has The final part of the survey assessed the participants’ totally disappeared after the awareness campaign, in a knowledge about antibiotic resistance. We found that demonstration of the health belief model [30]. Overall, almost 70% of the participants had already heard about these data show that even in a population that is relatively antibiotic resistance more than once and from different well informed, awareness campaigns can help change sources, mainly healthcare professionals and from media public understanding of the problems posed by AMR. sources. This figure is almost 3 times higher than in the This is echoed by a systematic review showing that inter - WHO report (22%) [26] and around twice as high as pre- ventions to raise antibiotic awareness among the public viously found in Egypt (40%) [27]. This shows that the in the USA improved knowledge, attitudes and behaviour repetition of the message alone might not be enough to [31]. promote behaviour change. Moreover, whereas 11% of Maarouf et al. Antimicrobial Resistance & Infection Control (2023) 12:50 Page 7 of 9 While the awareness campaign was quite effective at awareness campaign resulted in reduction in the number changing the views and understanding of participants of participants that would take an antibiotic whenever (views were changed in 10 out of 13 questions) there is they have an infection which is indicative of improved still clearly work to be done to improve public knowl- attitudes. Subjective norms are explained here by the edge. For example, despite the awareness campaign, 1 in participants’ perception of whether people important to 5 participants still believed a more expensive antibiotic them would use or ask for an antibiotic. In the current would be better for them, and would self-medicate, while study the finding that the participants were more likely 8% believed they should be taking more antibiotics rather to tell others about antibiotics following the educational than fewer. It is possible that these represent people who intervention is an indication of a positive impact on their are more resistant to change. Our study population con- subjective norms. sisted largely of adults of an age at which their views and Finally, perceived behavioural control is exemplified behaviours will have been embedded for some time, and here by the difficulty level of obtaining an antibiotic. The which are harder to change than those of much younger finding that following the awareness session participants people [32]. When properly designed, education on anti- were not more likely to embrace a restriction to their abil- biotic resistance may be more effective in children [ 33], ity to obtain antibiotics on demand responds to the per- who are more open to new concepts and have had less ceived behavioural control. In future campaigns this can exposure to pre-existing misconceptions. This work also be addressed by stressing the benefits of restricting anti - stresses the importance of a multi-tiered approach com- biotic use in limiting antibiotic resistance development. bining educational interventions and peer influence tar - geting healthcare professionals and patients, as well as Conclusions regulatory enforcement. It is of particular note that of In conclusion, the tested population had some good pre- the three questions for which there was no difference in existing knowledge and attitudes to antibiotics and anti- responses following the awareness campaign, two were biotic resistance, but this was still increased as a result related to direct effects on individual choice and free - of the awareness campaign, with some incorrect percep- dom – there was no change in the number of people who tions corrected. However, some misconceptions persisted felt they should be able to buy antibiotics whenever they in a small proportion of the population, and this propor- liked, and no change in how often people felt they per- tion would likely be higher in a population with less pre- sonally should take antibiotics. This would appear to be existing knowledge. Hence, we recommended increasing in contradiction to the answers given to other questions, awareness campaigns for the public with customized such as 100% of participants post awareness believing engagement materials and activities that are more likely that unnecessary antibiotic use will adversely affect them to enable individuals to identify changes they could make and/or others. It is likely that this is due to the phenome- in their own behaviour. non that while people can understand an issue and agree To the best of the authors’ knowledge this is the sec- that certain behaviours at a population level need to ond published campaign to address the wise use of anti- change, they don’t believe that they should be restricted biotics among the general public in Egypt and the first in from access to a certain service if it is deemed inappro- Alexandria. priate by public health standards. This responds to the The main limitation of this study is that convenience perceived behavioural control construct of the theory of sampling was used to enroll participants resulting in a planned behaviour (TPB) explained below [34]. When relatively high level of education. Future studies might designing awareness campaigns, consideration should address this by replicating and expanding on this work be given to how people can be engaged at an individual, with patients of lower educational levels. Selection bias more personal level to enable them to identify how they resulting from potential differences between the groups could alter their own behaviour. A focus of future cam- before and after the awareness campaign is a potential paigns may be on potential harm of nonindicated antibi- limitation. Second, social desirability bias might have otics to the targeted individual rather than societal harm impacted the reported rates. Third, the study used a sin - resulting from antibiotic resistance in general [35]. gle approach to improve antibiotic use and that is raising The findings of the current study are aligned with the public awareness and didn’t address other forms and/or TPB that explains all behaviours that people control and levels of interventions. Finally, despite targeting a specific that has been used to explain many health behaviours. It group so that we could reassess their knowledge at subse- consists of a number of key constructs: (a) attitudes, (b) quent visits to the clubs, it was difficult to persuade par - subjective norms and (c) perceived behavioural control. ticipants to re-do the survey leading to a much smaller These components determine the behavioural inten - group number following the awareness campaign. We tion of a person [36]. In the current context, attitudes do not anticipate differences among the before and after are exemplified by using or asking for antibiotics; the awareness groups in relation to key study variables. In Maarouf et al. Antimicrobial Resistance & Infection Control (2023) 12:50 Page 8 of 9 Competing interests future work, we need to consider how to better incentiv- The authors declare that they have no competing interests. ise this. Received: 24 August 2022 / Accepted: 5 May 2023 List of Abbreviations AMR Antimicrobial Resistance EAAD European Antibiotic Awareness Day XDR Extensive Drug-Resistant MDR Multi Drug-Resistant References MRSA Methicillin Resistant Staphylococcus aureus 1. Organization WH. Antimicrobial Resistance: Global Report on Surveillance OTC Over The Counter 2014 [Available from: https://apps.who.int/iris/handle/10665/112642. PDR Pan Drug-Resistant 2. Aslam B, Wang W, Arshad MI, Khurshid M, Muzammil S, Rasool MH, et TPB T heory of Planned Behaviour al. Antibiotic resistance: a rundown of a global crisis. Infect Drug Resist. UK United Kingdom 2018;11:1645–58. USA Unit ed States of America 3. Ventola CL. The antibiotic resistance crisis: part 1: causes and threats. P T. WHO W orld Health Organization 2015;40(4):277–83. 4. Magiorakos AP, Srinivasan A, Carey RB, Carmeli Y, Falagas ME, Giske CG, et al. Multidrug-resistant, extensively drug-resistant and pandrug-resistant Supplementary Information bacteria: an international expert proposal for interim standard definitions for The online version contains supplementary material available at https://doi. acquired resistance. Clin Microbiol infection: official publication Eur Soc Clin org/10.1186/s13756-023-01249-5. Microbiol Infect Dis. 2012;18(3):268–81. 5. Review on Antimicrobial Resistance. Tackling drug-resistant infections glob- Additional File 1. Examples of educational flyers used by the clinical phar - ally: final report and recommendations. 2016. macy students in the awareness campaign. 6. Machongo RB, Mipando ALN. I don’t hesitate to use the left-over antibiotics for my child” practices and experiences with antibiotic use among caregivers Additional File 2. The Arabic version of the questionnaire used to assess of paediatric patients at Zomba central hospital in Malawi. BMC Pediatr. the participants’ knowledge, attitudes and behaviour towards antibiotic 2022;22(1):466. use and antibiotic resistance. 7. Voidăzan S, Moldovan G, Voidăzan L, Zazgyva A, Moldovan H. Knowledge, Attitudes and Practices regarding the use of antibiotics. Study on the General Additional File 3. The English translation of the questionnaire used to Population of Mureş County, Romania. Infect Drug Resist. 2019;12:3385–96. assess the participants’ knowledge, attitudes and behaviour towards 8. Endashaw Hareru H, Sisay D, Kassaw C, Kassa R. Antibiotics non-adherence antibiotic use and antibiotic resistance. and its associated factors among households in southern Ethiopia. SAGE Open Medicine. 2022;10:20503121221090472. 9. Sirota M, Round T, Samaranayaka S, Kostopoulou O. Expectations for antibiot- Acknowledgements ics increase their prescribing: causal evidence about localized impact. Health The authors would like to acknowledge clinical pharmacy students, Alexandria psychology: official journal of the Division of Health Psychology American University (classes 2021 and 2022) for their role in conducting the survey and Psychological Association. 2017;36(4):402–9. awareness campaign. 10. Amin MEK, Amine A, Newegy MS. Perspectives of pharmacy staff on dispens - ing subtherapeutic doses of antibiotics: a theory informed qualitative study. Author Contribution Int J Clin Pharm. 2017;39(5):1110–8. LM: Collection of survey data, administration of the awareness campaign, data 11. Aboulmagd E, Kassem MA, Abouelfetouh A. Global Landscape in Microbial analysis and interpretation, writing of the first draft. MA: data interpretation, Resistance. In: Ghazi I, Cawley M, editors. 21st Century Challenges in Antimi- writing of the manuscript. BE: Conceptualization, data analysis and crobial Therapy and Stewardship. Frontiers in anti-infective agents. Volume 3. interpretation, writing of the manuscript. AA: Conceptualization, supervision Singapore: Bentham Science Publishers Pte. Ltd.; 2020. pp. 1–21. of the survey data collection and awareness campaign, data analysis and 12. Sanchez GV, Roberts RM, Albert AP, Johnson DD, Hicks LA. Eec ff ts of knowl - interpretation, writing of the manuscript. All authors revised the manuscript edge, attitudes, and practices of primary care providers on antibiotic selec- and approved of the final form. tion, United States. Emerg Infect Dis. 2014;20(12):2041–7. 13. Stivers T, Mangione-Smith R, Elliott MN, McDonald L, Heritage J. Why do Funding physicians think parents expect antibiotics? What parents report vs what The authors would like to acknowledge funding received from UEA Vice physicians believe. J Fam Pract. 2003;52(2):140–8. Chancellor’s Global Challenges Research Fellowships fund awarded to Alaa 14. Byrne MK, Miellet S, McGlinn A, Fish J, Meedya S, Reynolds N, et al. The drivers Abouelfetouh and DFG (ZI 665/3 − 1 awarded to Alaa Abouelfetouh). The of antibiotic use and misuse: the development and investigation of a theory funders had no role in study design, collection, analysis and interpretation of driven community measure. BMC Public Health. 2019;19(1):1425. data or in manuscript writing. 15. Hashem RA, Yassin AS, Zedan HH, Amin MA. Fluoroquinolone resistant mechanisms in methicillin-resistant Staphylococcus aureus clinical isolates in Data Availability Cairo, Egypt. J Infect Dev Ctries. 2013;7(11):796–803. The datasets generated and analysed in the current study are available from 16. Alseqely M, Newton-Foot M, Khalil A, El-Nakeeb M, Whitelaw A, Abouelfetouh the corresponding author upon reasonable request. A. Association between fluoroquinolone resistance and MRSA genotype in Alexandria, Egypt. Sci Rep. 2021;11(1):4253. Declarations 17. El Kholy A, Baseem H, Hall GS, Procop GW, Longworth DL. Antimicrobial resistance in Cairo, Egypt 1999–2000: a survey of five hospitals. J Antimicrob Ethics approval and consent to participate Chemother. 2003;51(3):625–30. The study was approved by the Faculty of Medicine and Health Sciences 18. Abouelfetouh A, Torky AS, Aboulmagd E. Role of plasmid carrying bla NDM Research Ethics Committee, University of East Anglia (Reference 201819–102), in mediating antibiotic resistance among Acinetobacter baumannii clinical and The Research Ethics Committee at the Faculty of Pharmacy, Alexandria isolates from Egypt. 3 Biotech. 2020;10(4):170. University prior to study commencement. All potential study participants 19. Abdelaziz AI, Tawfik AG, Rabie KA, Omran M, Hussein M, Abou-Ali A et al. were provided with a participant information sheet prior to taking part in Quality of Community Pharmacy Practice in Antibiotic Self-Medication the study, and informed consent was obtained from all participants for the Encounters: A Simulated Patient Study in Upper Egypt. 2019;8(2). collection and use of their data before beginning the study. 20. Dooling KL, Kandeel A, Hicks LA, El-Shoubary W, Fawzi K, Kandeel Y, et al. Understanding antibiotic use in Minya District, Egypt: Physician and Phar- Consent for publication macist Prescribing and the factors influencing their Practices. Antibiot (Basel Not applicable. Switzerland). 2014;3(2):233–43. Maarouf et al. Antimicrobial Resistance & Infection Control (2023) 12:50 Page 9 of 9 21. Amin ME, Amine A, Newegy MS. Injudicious Provision of Subtherapeutic 30. Rosenstock IM. The Health Belief Model and Preventive Health Behavior. Doses of Antibiotics in Community Pharmacies. Innovations in Pharmacy. Health Educ Monogr. 1974;2(4):354–86. 2017;8(1). 31. Burstein VR, Trajano RP, Kravitz RL, Bell RA, Vora D, May LS. Communication 22. Kandeel A, Palms DL, Afifi S, Kandeel Y, Etman A, Hicks LA, et al. An interventions to promote the public’s awareness of antibiotics: a systematic educational intervention to promote appropriate antibiotic use for acute review. BMC Public Health. 2019;19(1):899. respiratory infections in a district in Egypt- pilot study. BMC Public Health. 32. Tucker JS, Klein DJ, Elliott MN. Social Control of Health Behaviors: a compari- 2019;19(Suppl 3):498. son of Young, Middle-Aged, and older adults. The Journals of Gerontology: 23. Cross EL, Tolfree R, Kipping R. Systematic review of public-targeted com- Series B. 2004;59(4):P147–P50. munication interventions to improve antibiotic use. J Antimicrob Chemother. 33. Appiah B, Anum-Hagin D, Gyansa-Luterrodt M, Samman E, Agyeman FKA, 2017;72(4):975–87. Appiah G et al. Children against antibiotics misuse and antimicrobial resis- 24. Mason T, Trochez C, Thomas R, Babar M, Hesso I, Kayyali R. Knowledge and tance: assessing effectiveness of storytelling and picture drawing as public awareness of the general public and perception of pharmacists about antibi- engagement approaches. Wellcome Open Research. 2021;6. otic resistance. BMC Public Health. 2018;18(1):711. 34. Ajzen I. The theory of planned behavior. Organ Behav Hum Decis Process. 25. Yasmeen BN. The first World Antibiotic Awareness Week on Antibiotic Resis - 1991;50(2):179–211. tance. North Int Med Coll J. 2016;7(2):123–4. 35. Miller BJ, Carson KA, Keller S. Educating patients on unnecessary antibiotics: 26. Organization WH. Antibiotic resistance: Multi-country public awareness personalizing potential harm aids patient understanding. J Am Board Family survey. 2015. Medicine: JABFM. 2020;33(6):969–77. 27. Mostafa A, Abdelzaher A. Is health literacy associated with antibiotic use, 36. Ajzen I. The theory of planned behavior: frequently asked questions. Hum knowledge and awareness of antimicrobial resistance among non-medical Behav Emerg Technol. 2020;2(4):314–24. university students in Egypt? A cross-sectional study. 2021;11(3):e046453. 28. Shirai M. Impact of “High quality, low Price” appeal on consumer evaluations. Publisher’s Note J Promotion Manage. 2015;21(6):776–97. Springer Nature remains neutral with regard to jurisdictional claims in 29. McNulty CAM, Collin SM, Cooper E, Lecky DM, Butler CC. Public understand- published maps and institutional affiliations. ing and use of antibiotics in England: findings from a household survey in 2017. BMJ Open. 2019;9(10):e030845–e. http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Antimicrobial Resistance and Infection Control Springer Journals

Knowledge, attitudes and behaviour of Egyptians towards antibiotic use in the community: can we do better?

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Abstract

Background Infectious diseases are among the leading causes of death worldwide. This is concerning because of the increasing capacity of the pathogens to develop antibiotic resistance. Antibiotic overuse and misuse remain the main drivers of resistance development. In the USA and Europe, annual campaigns raise awareness of antibiotic misuse hazards and promote their judicial use. Similar efforts are lacking in Egypt. This study assessed the knowledge of the public in Alexandria, Egypt of antibiotic misuse risks and their habits towards antibiotic use, in addition to conducting a campaign to increase awareness of the safe use of antibiotics. Methods A questionnaire assessing knowledge, attitudes and behaviour towards antibiotics was used to collect responses from study participants at various sports clubs in Alexandria in 2019. An awareness campaign to correct misconceptions and a post awareness survey followed. Results Most of the participants were well-educated (85%), in their middle age (51%) and took antibiotics last year (80%). 22% would take an antibiotic for common cold. This dropped to 7% following the awareness. There was a 1.6 time increase in participants who would start an antibiotic on a healthcare professional’s advice following the campaign. A 1.3 time increase in participants who would finish an antibiotic regimen was also observed. The campaign made all participants recognize that unwise antibiotic use is harmful to them or others; and 1.5 more participants would spread the word about antibiotic resistance. Despite learning of the risks of antibiotic use, there was no change in how often participants thought they should take antibiotics. Conclusions Although awareness of antibiotic resistance is rising, some wrong perceptions hold fast. This highlights the need for patient and healthcare-tailored awareness sessions as part of a structured and national public health program directed to the Egyptian population. Keywords Antibiotic resistance, Awareness campaign, Educational intervention, Common cold, The theory of planned behaviour *Correspondence: Department of Pharmacy Practice and Clinical Pharmacy, Faculty of Alaa Abouelfetouh Pharmacy, Alamein International University, New Alamein City alaa.abouelfetouh@pharmacy.alexu.edu.eg 51718, Egypt 1 4 Department of Microbiology and Immunology, Faculty of Pharmacy, Department of Microbiology and Immunology, Faculty of Pharmacy, Alexandria University, 1 Khartoum Sq, Azarita, Alexandria 21521, Egypt Alamein International University, New Alamein City 51718, Egypt Norwich Medical School, University of East Anglia, Norwich, UK © The Author(s) 2023. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Maarouf et al. Antimicrobial Resistance & Infection Control (2023) 12:50 Page 2 of 9 Background Kholy et al. found that around 70% of Staphylococcus Antimicrobial resistance (AMR) represents a serious aureus isolates were resistant to a wide range of antibi- problem described by the World Health Organization otic classes. Another study reported fluoroquinolone (WHO) as “a global public health concern” [1]. AMR resistance among methicillin-resistant S. aureus (MRSA) has dire consequences worldwide as it increases mor- isolates from Alexandria, Egypt to range between 78% bidity and mortality rates from bacterial infection and and 96% [16]. Among Gram negative pathogens, 94% mandates quick interventions to mitigate the problem of E. coli isolates were resistant to ampicillin [17] and [2]. In the last three decades, the rate of approval of new upward of 70% of Acinetobacter baumannii isolates from antibiotics has slowed while antibiotic resistant bacte- Alexandria Main University Hospital were MDR [18]. rial pathogens have continued to emerge [3]. Moreover, However, only a small number of studies reported the pathogens keep acquiring more resistance determinants percentage of antibiotic misuse among Egyptian com- leading to the emergence of multidrug-resistant (MDR) munity pharmacies. Abdelaziz et al. reported that 98% of and even extensive drug-resistant (XDR) and pan drug- the visited pharmacies dispensed an antibiotic as an over resistant (PDR) bacteria which are resistant to all antibi- the counter (OTC) drug to treat ‘flu symptoms’ [ 19]. In otics [4]. another report, Dooling et al. mentioned that 64% and The emergence of these resistant bacteria leads to 81% of participating physicians and pharmacists, respec- a socioeconomic burden worldwide due to increased tively, from Minya, Egypt were prescribing antibiotics for healthcare costs as a result of using more expensive anti- patients with symptoms consistent with a common cold microbials and prolonged hospital stays, in addition to [20]. Moreover, a “cold group” that is a combination of lost productivity. It is estimated that the annual health pills, that may contain antibiotics, and that is commonly burden of the treatment of MDR bacterial infections in sold in some Egyptian pharmacies to treat common cold the USA is around $20 billion, with $35 billion lost due to was provided to simulated clients in 28.7% of the cases. reduced productivity [3], and a global annual death toll of In all of these, the cold group contained one or more 700,000 in 2014 that is expected to increase to 10 million antibiotic pills [21]. by 2050 [5]. Patient pressure has been identified as an important Research from around the globe indicates high rates driver for injudicious prescribing and dispensing of anti- of injudicious use of antibiotics by the public. Practices biotics, yet a lone campaign in Minya, Egypt promoted related to injudicious use in the literature include the use the appropriate use of antibiotics to treat respiratory tract of left over antibiotics [6, 7] and antibiotic non-adherence infections among prescribers and the general public [22]. usually due to remission of symptoms [8]. Further, the The aim of the current work was to assess the knowledge pressure made by patients who request antibiotics from of antibiotic resistance among the public in Alexandria, clinicians has been shown to be one of the factors driving Egypt and their attitudes towards antibiotic use. More- unwarranted provision of antibiotics by clinicians such over, an awareness campaign was designed to educate the as physicians [9] and pharmacists [10]. Antibiotic abuse participants on appropriate antibiotic use principles. The and misuse in the form of overuse or underuse remain knowledge was re-assessed at the conclusion of the cam- some of the most important factors contributing to paign to measure its effectiveness. In order to achieve resistance development particularly in developing coun- these aims we targeted the parents of children attending tries (reviewed in [11]). A study investigating the driv- sports clubs, as this would allow us to repeatedly inter- ers of antibiotic use and misuse in the community found act with the same individuals over the course of several patient behaviour to be an important driving factor. This weeks. To the best of the authors’ knowledge, this is the takes the form of patients putting pressure on a physician second published awareness campaign in Egypt and the to prescribe an unnecessary antibiotic either directly by first in Alexandria to address wise antibiotic use among demanding an antibiotic or indirectly when questioning the general public. the absence of an antibiotic in a prescription [12, 13]. Moreover, many patients believe they have the right to Methods self-prescribe an antibiotic or get one from friends and A questionnaire was used to collect responses from study family [14]. About 50% of antibiotic use is done improp- participants who were the parents of children playing erly in the form of using the wrong agent or the wrong sports at different sports clubs in Alexandria, Egypt. The dose or duration (reviewed in [11]). study was conducted over three months between July and In Egypt, antibiotic misuse and overuse led to a high September 2019. It was divided into three phases. Phase prevalence of MDR bacteria among the population one consisted of a general survey about participant’s anti- (reviewed in [15]). Most studies comment on the resis- biotic use and knowledge of antibiotic resistance. Phase tance rates among a particular MDR pathogen rather two consisted of an antibiotic awareness campaign to than on the general prevalence of MDR organisms. El guide people against the misuse of antibiotics and its Maarouf et al. Antimicrobial Resistance & Infection Control (2023) 12:50 Page 3 of 9 consequences on antibiotic resistance, and phase three Data analysis consisted of a post awareness questionnaire to assess the The data were tabulated and statistically analysed using effectiveness of the awareness sessions. The awareness Fisher’s exact test and Chi squared test, where the results sessions were delivered by Alexandria University clinical were considered significant at a p value of ≤ 0.05. The pharmacy students and took the form of informal chats Independent variable was the education, and the depen- with the participants. As part of the sessions, the partici- dent variables were knowledge and attitudes towards pants were given some flyers (Additional File 1) stressing antibiotic use and resistance. Categorical variable was the awareness messages. The students took turns deliver - classified to Zero (unexposed to education), 1 (exposed ing the messages and used the flyers as guiding points. to education). Data showing significant differences were Ethical approval for the study was obtained from the subsequently analysed by binary or multinomial logistic Faculty of Medicine and Health Sciences Research Eth- regression in SPSS (v. 28.0.1.1) to obtain odds ratios. For ics Committee, University of East Anglia (Reference multinomial regression, the reference category was set as 201,819–102), and The Research Ethics Committee at the the largest category for each dataset. Faculty of Pharmacy, Alexandria University prior to study commencement. Results A total of 626 sports club attendees were approached Sampling and they all agreed to participate in the study making Convenience sampling was used to recruit the partici- the response rate 100%. The majority of the participants pants. No specific sample size was designated before (51%) were aged 31 to 50 years old, 76% of the partici- study commencement. The sample size was determined pants were females and 85% were university graduates in light of the number of students contributing to the holding a bachelor or a higher degree. campaign. The students set up working stations on week - Surveying the history of antibiotic use showed that days and weekends in each of the sports clubs they vis- more than 80% of the participants took antibiotics last ited and approached all adults who came in contact with year at least once, with 46% taking antibiotics 2 to 3 them. All potential study participants were provided with times. Of those who had taken antibiotics, 80% took them a participant information sheet prior to taking part in the on the advice of a healthcare professional (62% from a study, and informed consent was obtained from all par- doctor, 18% from a pharmacist), while 20% took them ticipants for the collection and use of their data before after advice from non-healthcare professional sources beginning the study. The participants were then given the (13% decided themselves, 6% from a family member, 1% paper-based questionnaire by the students. The partici - from a friend) (Table  1). On the other hand, more than pants returned the completed questionnaire back to the 50% of the participants said that they were informed by students when they were done. their physician that they don’t need an antibiotic to treat their symptoms, yet > 80% of the participants took antibi- Design of the questionnaire otics in the previous year. The questionnaire (Additional File 2 shows the Arabic Looking at participant knowledge of antibiotic use, 35% version and Additional File 3 shows the English transla- of the participants believed that more expensive antibiot- tion) covered the demographic and professional data of ics would be more effective. This percentage was almost the participants and then was divided into two parts. The halved following the campaign (binary logistic regression, first part consisted of six questions collecting data about OR = 0.431, 95% CI = 0.196–0.945, p = 0.036). A total of past antibiotic use. The second part contained 13 ques - 78% of the participants thought that they should not take tions about knowledge and attitudes towards antibiotics antibiotics for a common cold; this percentage increased and antibiotic resistance. The participants were asked to 93% after the campaign (binary logistic regression, to fill both parts of the questionnaire at phase one, and OR = 0.255, 95% CI = 0.078–0.837, p = 0.024). Yet, almost just the second part at phase three following the aware- half of the participants would start an antibiotic based on ness campaign. The full questionnaire needed an average their own assessment of their symptoms versus 34% who of five minutes to be completed. A pilot study covering would start an antibiotic following advice from a physi- over 500 participants had been carried out prior to cur- cian or pharmacist. These percentages changed to 20% rent data collection. and 55% following the awareness campaign (Chi squared The questionnaire was anonymous, the demographic test, p < 0.001). Nevertheless, 64% of the participants data collected can’t be used to determine the identity of knew that they should complete the antibiotic regimen, the participants, and therefore the data from phase one which increased to 86% as a consequence of the aware- and phase three can’t be linked to individuals. ness campaign (Chi squared test, p < 0.001) (Table 2). Concerning participants’ attitudes towards antibiotic use, only 18% reported that they would put pressure on Maarouf et al. Antimicrobial Resistance & Infection Control (2023) 12:50 Page 4 of 9 Table 1 Participant demographics and antibiotic use in the test, p < 0.001). As for participant’ attitudes towards anti- previous year biotic resistance, 87% have now told others about anti- Number Percentage biotic resistance versus just 59% before the campaign Age group (years) 192 30.7 (binary logistic regression, OR = 4.729, 95% CI = 1.818– 18–30 320 51.1 12.301, p = 0. 001), yet the campaign does not seem to 31–50 92 14.7 have changed how often people would take an antibiotic 51–70 22 3.5 > 70 (Table 3). Gender 478 76.4 Female 146 23.3 Discussion Male 2 0.3 Antibiotic resistance, which is a worldwide crisis, is a Prefer not to say crucial problem; and urgent action is needed to resolve Level of education 95 15.2 it. One of the important pillars in combatting AMR is Postgraduate 435 69.5 improving public knowledge of antibiotic use [23]. Glob- Bachelor 85 13.6 High school graduate 10 1.6 ally, many antibiotic awareness campaigns have been Middle school graduate 1 0.2 conducted to increase public understanding of the risks None around the misuse of antibiotics and the threat from Antibiotic use in last year 184 35.5 antibiotic resistance. For instance, European Antibiotic Once 241 46.4 Awareness Day (EAAD), which was launched in 2008 is 2–3 times 94 18.1 an annual event co-ordinating public engagement activi- ≥ 4 times Who advised you to take the antibiotics? 345 62.4 ties across Europe [24], and World Antibiotic Awareness Doctor 99 17.9 Week, which was firstly introduced by WHO in 2015, is Pharmacist 0 0 held in the middle of November annually [25]. Therefore, Nurse 6 1.1 this study aimed to assess public knowledge and then Friend 31 5.6 determine the impact of an awareness campaign designed Family member 70 12.7 Self 2 0.4 to provide the public with information about appropriate Other antibiotic use and the problem of resistance. Promising findings from this study are in line with recent research the physician to prescribe an antibiotic, which dropped in Egypt showing an improvement in prescribing habits, to 7% after the campaign (Fisher’s exact test, p = 0.031; attitude and belief scores for physicians, pharmacists, and binary logistic regression, OR = 0.353, 95% CI = 0.107– patients regarding antibiotic use following a campaign in 1.162, p = 0.087). While there was also a significant drop Minya, a governorate in Southern Egypt [22]. in the number of participants who would buy antibiotics Although the sample size was not pre-determined and to use even if a doctor hadn’t told them they needed them it mainly depended on the number of students deliver- (34% before the awareness campaign vs. 17% after; binary ing the survey and awareness campaign, given the large logistic regression, OR = 0.409, 95% CI = 0.178–0.938, number of participants in the study and the significance p = 0.035), there remained a substantial number of peo- of findings we do not anticipate that inadequate power ple who would still purchase antibiotics. This was further was to be an issue of concern. In general, most of the reflected in the fact that there was no significant differ - tested population (85%) used antibiotics throughout ence in the number of participants who felt they should the last year, which is almost the same percentage (89%) be able to buy antibiotics whenever they want them, with described in a recent WHO report [26] that studied anti- almost one in three participants wanting the freedom to biotic use in different countries including Egypt. 80% do so (Table 2). of the participants had been prescribed antibiotics by Regarding antibiotic resistance, 78% of participants healthcare professionals, and only 13% were self-medi- had already heard about the problem even before the cated; this percentage is lower than previously reported campaign; this occurred through interaction with a by WHO (26%) [26] and in an Egyptian study on non- healthcare practitioner in 47% of cases and through the medical students (39%) [27]. This could be explained by media in 33% (Table 3). It is of note that as many people the high percentage of well-educated participants in our had heard about antibiotic resistance from a physician study who also tend to be wealthier. As such, they could or a nurse as had heard about it from the media (33% in afford to consult with healthcare professionals rather both cases). Despite hearing about antibiotic resistance, than being forced to self-medicate. about 11% thought that unwise antibiotic use won’t have Moreover, one third of participants believed that the a harmful effect. Following the awareness campaign, more expensive an antibiotic is, the more effective it is. 100% of the participants appreciated that resistance is a This could be explained by the perception in general that problem for everyone now and in the future (Chi squared any product with a higher price will be higher in quality, Maarouf et al. Antimicrobial Resistance & Infection Control (2023) 12:50 Page 5 of 9 Table 2 Participant knowledge and attitudes towards antibiotics before and after the awareness sessions Participant knowledge Before After p value Regression awareness awareness n % n % p value Odds Lower Upper ratio 95% 95% CI CI Do you believe more expensive antibiotics are more 216 34.7 8 18.6 0.011455 0.036 0.431 0.196 0.945 likely to make you feel better? 407 65.3 35 81.4 Yes No Do you believe you have to take an antibiotic when- 139 22.3 3 7 0.004288 0.024 0.255 0.078 0.837 ever you have an infection, like a cold? 483 77.7 40 93 Yes No When you get a cold, when do you think you should 88 14.1 11 25 2.67021E-07 0.845 1.078 0.506 2.296 start taking antibiotics? 71 11.4 3 6.8 0.108 0.364 0.107 1.247 I don’t take them 124 19.9 4 9.1 0.02 0.278 0.094 0.821 When feeling the first symptoms of a cold 105 16.8 2 4.5 0.015 0.164 0.038 0.708 After cough and sputum appear 207 33.2 24 54.5 Ref - - - After the colour of mucous changes 1 0.2 0 0 - - - - After a doctor or pharmacist tells me to take one 18 2.9 0 0 - - - - I have never had a cold 10 1.6 0 0 - - - - I don’t know Others When you have been taking antibiotics, when do 202 32.5 5 11.6 6.41626E-05 0.006 0.266 0.103 0.686 you think you should stop the antibiotic treatment? 397 63.8 37 86 Ref - - - When I feel better 18 2.9 1 2.3 0.619 0.596 0.077 4.592 After I finish the full course 5 0.8 0 0 - - - - I have never taken antibiotics I don’t know Participant attitudes Before After p value  Regression awareness awareness n % n % p value  Odds  Lower Upper ratio 95% 95% CI CI  Would you ask a doctor to prescribe an antibiotic if 109 17.5 3 7 0.030886 0.087 0.353 0.107 1.162 you believe you need one, even if the doctor did not 513 82.5 40 93 think it was needed? Yes No Would you buy antibiotics to use without being told 208 33.5 7 17.1 0.013828 0.035 0.409 0.178 0.938 you need them by a doctor? 413 66.5 34 82.9 Yes No Do you think you should be able to buy antibiotics 188 30.3 11 26.8 0.642698 nd nd nd nd whenever you want them? 433 69.7 30 73.2 Yes No Ref indicates this is the reference category in multinomial logistic regression analyses. nd, not done as initial analysis reported no significant difference. Dashes (-) in p value, OR and 95% CI columns for multinomial regression represent non-returned values due to insufficient data. Answers to some questions were missing neglecting its actual properties [28]. However, as a result misconception, with only 7% of people saying they would of the campaign, this percentage was almost halved. take an antibiotic for a cold after taking part. Similarly, In total 22% of the participants believed that antibiotics concerning the completion of the antibiotic course, 64% could be used to treat the common cold, which is much of participants believed that they should complete their lower than found in the WHO’s report (76%) [26] and antibiotic course, which is high compared to the WHO close to what was published in a survey in 2017 in Eng- report (41%) [26]. However, this value increased to 86% land (15%) [29]. In these studies, the participants may not after the campaign, which comes near the rate described have been aware that the common cold is a viral infection in the English report (87%) [29]. The high level of aware - that could not be treated by antibiotics. Our awareness ness of the need to complete the antibiotic course seen campaign was particularly effective at correcting this Maarouf et al. Antimicrobial Resistance & Infection Control (2023) 12:50 Page 6 of 9 Table 3 Participant knowledge and attitudes towards antibiotic resistance before and after the awareness sessions Participant knowledge Before After p value Regression awareness awareness n % n % p value Odds Lower Upper ratio 95% 95% CI CI How many times have you heard about antibiotic 388 62.9 30 69.8 8.97963E-13 Ref - - - resistance? 43 7 0 0 - - - - Many times 50 8.1 11 25.6 0.006 2.845 1.343 6.03 A few times 136 22 2 4.7 0.024 0.19 0.045 0.806 Only once I don’t remember hearing about antibiotic resistance Where have you heard about antibiotic resistance? 167 33.2 6 15 3.41269E-32 0.594 0.746 0.253 2.195 From a physician or nurse 69 13.7 19 47.5 0.00009 5.714 2.388 13.672 From a pharmacist 70 13.9 5 12.5 0.503 1.482 0.468 4.689 From friends or family 29 5.8 0 0 - - - - At school/college/university 166 33 8 20 Ref - - - In the media (television, radio, newspapers, magazines 2 0.4 2 5 0.004 20.75 2.581 166.828 etc.) Others How widespread do you think antibiotic resistance is? 52 11 4 10.3 0.110692 nd nd nd nd Mostly found in rich countries 153 32.3 9 23.1 Mostly found in poor countries 269 56.8 26 66.7 Worldwide What do you think will happen if you use antibiotics 54 11 0 0 0.000175 - - - - unnecessarily? 211 42.9 18 46.2 Ref - - - Nothing 24 4.9 0 0 - - - - Antibiotic-resistant infections will personally affect me 203 41.3 21 53.8 0.566 1.213 0.628 2.342 Antibiotic-resistant infections will affect others in the future Antibiotic-resistant infections will affect me, and others in the future Participant attitudes Before After p value  Regression awareness awareness n % n % p value Odds  Lower Upper ratio  95% 95% CI CI  Has hearing about antibiotic resistance changed how 36 7.6 3 8.1 0.46244164 nd nd nd nd often you think you should take antibiotics? 352 74.1 29 78.4 Yes – I think I should take them more 87 18.3 5 13.5 Yes – I think I should take them less No Have you told anyone else about antibiotic resistance? 289 59 34 87.2 7.4E-06 0.001 4.729 1.818 12.301 Yes 201 41 5 12.8 No Ref indicates this is the reference category in multinomial logistic regression analyses. nd, not done as initial analysis reported no significant difference. Dashes (-) in p value, OR and 95% CI columns for multinomial regression represent non-returned values due to insufficient data. Answers to some questions were missing in the current study might be explained by the high per- participants thought that there will be no harmful effects centage of well-educated participants. from antibiotic resistance in the future, this concept has The final part of the survey assessed the participants’ totally disappeared after the awareness campaign, in a knowledge about antibiotic resistance. We found that demonstration of the health belief model [30]. Overall, almost 70% of the participants had already heard about these data show that even in a population that is relatively antibiotic resistance more than once and from different well informed, awareness campaigns can help change sources, mainly healthcare professionals and from media public understanding of the problems posed by AMR. sources. This figure is almost 3 times higher than in the This is echoed by a systematic review showing that inter - WHO report (22%) [26] and around twice as high as pre- ventions to raise antibiotic awareness among the public viously found in Egypt (40%) [27]. This shows that the in the USA improved knowledge, attitudes and behaviour repetition of the message alone might not be enough to [31]. promote behaviour change. Moreover, whereas 11% of Maarouf et al. Antimicrobial Resistance & Infection Control (2023) 12:50 Page 7 of 9 While the awareness campaign was quite effective at awareness campaign resulted in reduction in the number changing the views and understanding of participants of participants that would take an antibiotic whenever (views were changed in 10 out of 13 questions) there is they have an infection which is indicative of improved still clearly work to be done to improve public knowl- attitudes. Subjective norms are explained here by the edge. For example, despite the awareness campaign, 1 in participants’ perception of whether people important to 5 participants still believed a more expensive antibiotic them would use or ask for an antibiotic. In the current would be better for them, and would self-medicate, while study the finding that the participants were more likely 8% believed they should be taking more antibiotics rather to tell others about antibiotics following the educational than fewer. It is possible that these represent people who intervention is an indication of a positive impact on their are more resistant to change. Our study population con- subjective norms. sisted largely of adults of an age at which their views and Finally, perceived behavioural control is exemplified behaviours will have been embedded for some time, and here by the difficulty level of obtaining an antibiotic. The which are harder to change than those of much younger finding that following the awareness session participants people [32]. When properly designed, education on anti- were not more likely to embrace a restriction to their abil- biotic resistance may be more effective in children [ 33], ity to obtain antibiotics on demand responds to the per- who are more open to new concepts and have had less ceived behavioural control. In future campaigns this can exposure to pre-existing misconceptions. This work also be addressed by stressing the benefits of restricting anti - stresses the importance of a multi-tiered approach com- biotic use in limiting antibiotic resistance development. bining educational interventions and peer influence tar - geting healthcare professionals and patients, as well as Conclusions regulatory enforcement. It is of particular note that of In conclusion, the tested population had some good pre- the three questions for which there was no difference in existing knowledge and attitudes to antibiotics and anti- responses following the awareness campaign, two were biotic resistance, but this was still increased as a result related to direct effects on individual choice and free - of the awareness campaign, with some incorrect percep- dom – there was no change in the number of people who tions corrected. However, some misconceptions persisted felt they should be able to buy antibiotics whenever they in a small proportion of the population, and this propor- liked, and no change in how often people felt they per- tion would likely be higher in a population with less pre- sonally should take antibiotics. This would appear to be existing knowledge. Hence, we recommended increasing in contradiction to the answers given to other questions, awareness campaigns for the public with customized such as 100% of participants post awareness believing engagement materials and activities that are more likely that unnecessary antibiotic use will adversely affect them to enable individuals to identify changes they could make and/or others. It is likely that this is due to the phenome- in their own behaviour. non that while people can understand an issue and agree To the best of the authors’ knowledge this is the sec- that certain behaviours at a population level need to ond published campaign to address the wise use of anti- change, they don’t believe that they should be restricted biotics among the general public in Egypt and the first in from access to a certain service if it is deemed inappro- Alexandria. priate by public health standards. This responds to the The main limitation of this study is that convenience perceived behavioural control construct of the theory of sampling was used to enroll participants resulting in a planned behaviour (TPB) explained below [34]. When relatively high level of education. Future studies might designing awareness campaigns, consideration should address this by replicating and expanding on this work be given to how people can be engaged at an individual, with patients of lower educational levels. Selection bias more personal level to enable them to identify how they resulting from potential differences between the groups could alter their own behaviour. A focus of future cam- before and after the awareness campaign is a potential paigns may be on potential harm of nonindicated antibi- limitation. Second, social desirability bias might have otics to the targeted individual rather than societal harm impacted the reported rates. Third, the study used a sin - resulting from antibiotic resistance in general [35]. gle approach to improve antibiotic use and that is raising The findings of the current study are aligned with the public awareness and didn’t address other forms and/or TPB that explains all behaviours that people control and levels of interventions. Finally, despite targeting a specific that has been used to explain many health behaviours. It group so that we could reassess their knowledge at subse- consists of a number of key constructs: (a) attitudes, (b) quent visits to the clubs, it was difficult to persuade par - subjective norms and (c) perceived behavioural control. ticipants to re-do the survey leading to a much smaller These components determine the behavioural inten - group number following the awareness campaign. We tion of a person [36]. In the current context, attitudes do not anticipate differences among the before and after are exemplified by using or asking for antibiotics; the awareness groups in relation to key study variables. In Maarouf et al. Antimicrobial Resistance & Infection Control (2023) 12:50 Page 8 of 9 Competing interests future work, we need to consider how to better incentiv- The authors declare that they have no competing interests. ise this. Received: 24 August 2022 / Accepted: 5 May 2023 List of Abbreviations AMR Antimicrobial Resistance EAAD European Antibiotic Awareness Day XDR Extensive Drug-Resistant MDR Multi Drug-Resistant References MRSA Methicillin Resistant Staphylococcus aureus 1. Organization WH. Antimicrobial Resistance: Global Report on Surveillance OTC Over The Counter 2014 [Available from: https://apps.who.int/iris/handle/10665/112642. PDR Pan Drug-Resistant 2. Aslam B, Wang W, Arshad MI, Khurshid M, Muzammil S, Rasool MH, et TPB T heory of Planned Behaviour al. Antibiotic resistance: a rundown of a global crisis. Infect Drug Resist. UK United Kingdom 2018;11:1645–58. USA Unit ed States of America 3. Ventola CL. The antibiotic resistance crisis: part 1: causes and threats. P T. WHO W orld Health Organization 2015;40(4):277–83. 4. Magiorakos AP, Srinivasan A, Carey RB, Carmeli Y, Falagas ME, Giske CG, et al. Multidrug-resistant, extensively drug-resistant and pandrug-resistant Supplementary Information bacteria: an international expert proposal for interim standard definitions for The online version contains supplementary material available at https://doi. acquired resistance. Clin Microbiol infection: official publication Eur Soc Clin org/10.1186/s13756-023-01249-5. Microbiol Infect Dis. 2012;18(3):268–81. 5. Review on Antimicrobial Resistance. Tackling drug-resistant infections glob- Additional File 1. Examples of educational flyers used by the clinical phar - ally: final report and recommendations. 2016. macy students in the awareness campaign. 6. Machongo RB, Mipando ALN. I don’t hesitate to use the left-over antibiotics for my child” practices and experiences with antibiotic use among caregivers Additional File 2. The Arabic version of the questionnaire used to assess of paediatric patients at Zomba central hospital in Malawi. BMC Pediatr. the participants’ knowledge, attitudes and behaviour towards antibiotic 2022;22(1):466. use and antibiotic resistance. 7. Voidăzan S, Moldovan G, Voidăzan L, Zazgyva A, Moldovan H. Knowledge, Attitudes and Practices regarding the use of antibiotics. Study on the General Additional File 3. The English translation of the questionnaire used to Population of Mureş County, Romania. Infect Drug Resist. 2019;12:3385–96. assess the participants’ knowledge, attitudes and behaviour towards 8. Endashaw Hareru H, Sisay D, Kassaw C, Kassa R. Antibiotics non-adherence antibiotic use and antibiotic resistance. and its associated factors among households in southern Ethiopia. SAGE Open Medicine. 2022;10:20503121221090472. 9. Sirota M, Round T, Samaranayaka S, Kostopoulou O. Expectations for antibiot- Acknowledgements ics increase their prescribing: causal evidence about localized impact. Health The authors would like to acknowledge clinical pharmacy students, Alexandria psychology: official journal of the Division of Health Psychology American University (classes 2021 and 2022) for their role in conducting the survey and Psychological Association. 2017;36(4):402–9. awareness campaign. 10. Amin MEK, Amine A, Newegy MS. Perspectives of pharmacy staff on dispens - ing subtherapeutic doses of antibiotics: a theory informed qualitative study. Author Contribution Int J Clin Pharm. 2017;39(5):1110–8. LM: Collection of survey data, administration of the awareness campaign, data 11. Aboulmagd E, Kassem MA, Abouelfetouh A. Global Landscape in Microbial analysis and interpretation, writing of the first draft. MA: data interpretation, Resistance. In: Ghazi I, Cawley M, editors. 21st Century Challenges in Antimi- writing of the manuscript. BE: Conceptualization, data analysis and crobial Therapy and Stewardship. Frontiers in anti-infective agents. Volume 3. interpretation, writing of the manuscript. AA: Conceptualization, supervision Singapore: Bentham Science Publishers Pte. Ltd.; 2020. pp. 1–21. of the survey data collection and awareness campaign, data analysis and 12. Sanchez GV, Roberts RM, Albert AP, Johnson DD, Hicks LA. Eec ff ts of knowl - interpretation, writing of the manuscript. All authors revised the manuscript edge, attitudes, and practices of primary care providers on antibiotic selec- and approved of the final form. tion, United States. Emerg Infect Dis. 2014;20(12):2041–7. 13. Stivers T, Mangione-Smith R, Elliott MN, McDonald L, Heritage J. Why do Funding physicians think parents expect antibiotics? What parents report vs what The authors would like to acknowledge funding received from UEA Vice physicians believe. J Fam Pract. 2003;52(2):140–8. Chancellor’s Global Challenges Research Fellowships fund awarded to Alaa 14. Byrne MK, Miellet S, McGlinn A, Fish J, Meedya S, Reynolds N, et al. The drivers Abouelfetouh and DFG (ZI 665/3 − 1 awarded to Alaa Abouelfetouh). The of antibiotic use and misuse: the development and investigation of a theory funders had no role in study design, collection, analysis and interpretation of driven community measure. BMC Public Health. 2019;19(1):1425. data or in manuscript writing. 15. Hashem RA, Yassin AS, Zedan HH, Amin MA. Fluoroquinolone resistant mechanisms in methicillin-resistant Staphylococcus aureus clinical isolates in Data Availability Cairo, Egypt. J Infect Dev Ctries. 2013;7(11):796–803. The datasets generated and analysed in the current study are available from 16. Alseqely M, Newton-Foot M, Khalil A, El-Nakeeb M, Whitelaw A, Abouelfetouh the corresponding author upon reasonable request. A. Association between fluoroquinolone resistance and MRSA genotype in Alexandria, Egypt. Sci Rep. 2021;11(1):4253. Declarations 17. El Kholy A, Baseem H, Hall GS, Procop GW, Longworth DL. Antimicrobial resistance in Cairo, Egypt 1999–2000: a survey of five hospitals. J Antimicrob Ethics approval and consent to participate Chemother. 2003;51(3):625–30. The study was approved by the Faculty of Medicine and Health Sciences 18. Abouelfetouh A, Torky AS, Aboulmagd E. Role of plasmid carrying bla NDM Research Ethics Committee, University of East Anglia (Reference 201819–102), in mediating antibiotic resistance among Acinetobacter baumannii clinical and The Research Ethics Committee at the Faculty of Pharmacy, Alexandria isolates from Egypt. 3 Biotech. 2020;10(4):170. University prior to study commencement. All potential study participants 19. Abdelaziz AI, Tawfik AG, Rabie KA, Omran M, Hussein M, Abou-Ali A et al. were provided with a participant information sheet prior to taking part in Quality of Community Pharmacy Practice in Antibiotic Self-Medication the study, and informed consent was obtained from all participants for the Encounters: A Simulated Patient Study in Upper Egypt. 2019;8(2). collection and use of their data before beginning the study. 20. Dooling KL, Kandeel A, Hicks LA, El-Shoubary W, Fawzi K, Kandeel Y, et al. Understanding antibiotic use in Minya District, Egypt: Physician and Phar- Consent for publication macist Prescribing and the factors influencing their Practices. Antibiot (Basel Not applicable. Switzerland). 2014;3(2):233–43. Maarouf et al. Antimicrobial Resistance & Infection Control (2023) 12:50 Page 9 of 9 21. Amin ME, Amine A, Newegy MS. Injudicious Provision of Subtherapeutic 30. Rosenstock IM. The Health Belief Model and Preventive Health Behavior. Doses of Antibiotics in Community Pharmacies. Innovations in Pharmacy. Health Educ Monogr. 1974;2(4):354–86. 2017;8(1). 31. Burstein VR, Trajano RP, Kravitz RL, Bell RA, Vora D, May LS. Communication 22. Kandeel A, Palms DL, Afifi S, Kandeel Y, Etman A, Hicks LA, et al. An interventions to promote the public’s awareness of antibiotics: a systematic educational intervention to promote appropriate antibiotic use for acute review. BMC Public Health. 2019;19(1):899. respiratory infections in a district in Egypt- pilot study. BMC Public Health. 32. Tucker JS, Klein DJ, Elliott MN. Social Control of Health Behaviors: a compari- 2019;19(Suppl 3):498. son of Young, Middle-Aged, and older adults. The Journals of Gerontology: 23. Cross EL, Tolfree R, Kipping R. Systematic review of public-targeted com- Series B. 2004;59(4):P147–P50. munication interventions to improve antibiotic use. J Antimicrob Chemother. 33. Appiah B, Anum-Hagin D, Gyansa-Luterrodt M, Samman E, Agyeman FKA, 2017;72(4):975–87. Appiah G et al. Children against antibiotics misuse and antimicrobial resis- 24. Mason T, Trochez C, Thomas R, Babar M, Hesso I, Kayyali R. Knowledge and tance: assessing effectiveness of storytelling and picture drawing as public awareness of the general public and perception of pharmacists about antibi- engagement approaches. Wellcome Open Research. 2021;6. otic resistance. BMC Public Health. 2018;18(1):711. 34. Ajzen I. The theory of planned behavior. Organ Behav Hum Decis Process. 25. Yasmeen BN. The first World Antibiotic Awareness Week on Antibiotic Resis - 1991;50(2):179–211. tance. North Int Med Coll J. 2016;7(2):123–4. 35. Miller BJ, Carson KA, Keller S. Educating patients on unnecessary antibiotics: 26. Organization WH. Antibiotic resistance: Multi-country public awareness personalizing potential harm aids patient understanding. J Am Board Family survey. 2015. Medicine: JABFM. 2020;33(6):969–77. 27. Mostafa A, Abdelzaher A. Is health literacy associated with antibiotic use, 36. Ajzen I. The theory of planned behavior: frequently asked questions. Hum knowledge and awareness of antimicrobial resistance among non-medical Behav Emerg Technol. 2020;2(4):314–24. university students in Egypt? A cross-sectional study. 2021;11(3):e046453. 28. Shirai M. Impact of “High quality, low Price” appeal on consumer evaluations. Publisher’s Note J Promotion Manage. 2015;21(6):776–97. Springer Nature remains neutral with regard to jurisdictional claims in 29. McNulty CAM, Collin SM, Cooper E, Lecky DM, Butler CC. Public understand- published maps and institutional affiliations. ing and use of antibiotics in England: findings from a household survey in 2017. BMJ Open. 2019;9(10):e030845–e.

Journal

Antimicrobial Resistance and Infection ControlSpringer Journals

Published: May 24, 2023

Keywords: Antibiotic resistance; Awareness campaign, Educational intervention; Common cold; The theory of planned behaviour

References