Saba Hanif 1 BDS
Syeda Nadia Firdous2 BDS, MPH
Kauser Ismail3 BDS, M.Phil
Zoeen Fatima4 BDS
Angabeen Anjum5 BDS, M.Phil
OBJECTIVE: To evaluate the awareness and approach of dental students regarding antibiotic prescription and its resistance due to irrational use of antibiotics. Antibiotic resistance is spreading alarmingly throughout the world, including developed countries. The common causes of antibiotic resistance include over prescription, incomplete treatment and inappropriate selfmedication. Among different causes of antimicrobial resistance, irrational use of antibiotic is the most prominent one. METHODOLOGY: After approved by the Institutional Ethics Committee of Ziauddin University this cross-sectional study was conducted from 1st April, 2020 to 30th July,2020 at Ziauddin University. Third and final year dental students as well as house officers were enrolled and the computed sample size was 133 to which 5% non-response rate was added, therefore total 139 dental students were approached. Non-probability convenience sampling technique was used. A self- designed, selfadministered questionnaire was prepared to collect the demographic data and information regarding the prescription pattern of antibiotics amongst study subjects. All questions in the questionnaire were close ended. The questionnaire comprised information pertaining to demographic characteristics, standard guideline for antibiotic prescriptions, antibiotic stewardship and resistance, improper prescription and its consequences. The dental students were briefed about the purpose of the study and the significance of participation and a written informed consent was obtained from them. The awareness of dental students regarding antibiotics was the outcome factor. The data was analyzed by using SPSS version 22. RESULTS: Out of total 139 dental students majority (79.1%)were familiar to standard antibiotic prescription guidelines .(87.8%) responded amoxicillin is beta lactam, for probability of antibiotic abuse and antibiotics aid in recovery of infections majority showed awareness (92.1% and 84.9% respectively). Almost equal students inquire recent antibiotic course prior to prescription (90.6%) as well as take extra caution prescribing antibiotic in immune compromised patients (89.9%). CONCLUSION: This study concluded that majority of the dental students had good awareness regarding antibiotics and factors related to it, as participants responded positively to the 70% of awareness - based questions. KEYWORDS: Awareness. Antibiotics, Resistance, Prescription, Dental Students. HOW TO CITE: Hanif S, Firdous SN, Ismail K, Fatima Z, Anjum A. Assessment of awareness and approach regarding antibiotic prescription and resistance among different level of dental students in a tertiary care dental college, Karachi. J Pak Dent Assoc 2023;32(2):66-73. DOI: https://doi.org/10.25301/JPDA.322.66 Received: 22 August 2022, Accepted: 07 July 2023
In general practice, the cure of any disease is reliant on the use of drugs.1 Since the accidental discovery of penicillin by Alexander Fleming in 1928, antibioticshave been widely used in medical practice. Antibiotics are currently predominantly utilized in the obliteration of bacterial infections, either by killing them or slowing down their growth.2 However, according to one study, up to 50% of antibiotics are deemed unnecessary, and resistance is one of
the most serious challenges confronting medical practitioners.3
Antibiotic resistance occurs when microorganisms develop
a mechanism to protect themselves from antibiotics in order
to survive, rendering the antibiotic useless when used against
Antibiotic resistance is spreading alarmingly throughout the world, including developed countries.5 In recent years, it has been identified as one of the primary causes of a high frequency of hospitalization, morbidity, and mortality.6 According to current data, the World Health Organization (WHO) estimates that 700,000 people die each year as a result of antibiotic resistance, and predicts that by 2050, antimicrobial resistance will be responsible for ten million deaths per year.7 Multiple studies from the USA reported that at least 500,000 patients infected with C. difficile need to be admitted in hospital and <14,000 people died.8 Antimicrobial resistance data in middle- and low-income countries are limited because of the challenges in conducting antimicrobial resistance surveillance.9
The common causes of antibiotic resistance include over prescription, incomplete treatment and inappropriate selfmedication.10 Among different causes of antimicrobial resistance, irrational use of antibiotic is the most prominent one.11 Irrational antibiotics can take many forms, including the use of too many medicines per patient (polypharmacy), the inappropriate use of self-medication (often with prescription-only medicines), in non-bacterial infections, outside clinical guidelines, or with inadequate dosage or inappropriate route of administration such as overuse of injections when oral formulations would be more appropriate.12 The irrational drug has many bad consequences including treatment failure, compromise in patient health, and increased cost.13
Even in dentistry, antibiotic prescription for dental infection is a common practice. A study evealed that 12% of dentists adequately prescribed antibiotics as a prophylactic intervention and treatment.14 A study conducted in Australia revealed that antibiotics are not used vigilantly for various dental infections which has led to development of resistance.15 A study conducted in Karachi revealed that antibiotic
prescription has been increased to 65% in past ten years in low middle-income countries like Pakistan. 1 6 The World health Organization defines rational drug
prescription as the use of fewest number of drugs to achieve the best potential impact in the shortest time and at the lowest possible cost.17 It is fact that appropriate antibiotic selection, dose and duration of treatment could prevent or slow down the emergence of antimicrobial resistance.18 The change in doctors’ attitude have impact on the practice of their antibiotic prescription. Furthermore, if the doctors are aware of their practices regarding antibiotics prescription, they will grasp the guideline accordingly.19
To highlight the awareness about antibiotics use and to combat its resistance numerous agencies are in operation.20,21 Moreover, the World Health Organization (WHO) has recently focused on educating health care providers about proper prescription with step-by-step guideline.22
Antibiotic stewardship is a key intervention to improve prescribing practices at individual as well as combined professional level.23 Infectious Disease Society of America (IDSA) defined ‘antimicrobial stewardship’ as that optimizes the indication, selection, dosing, routes of administration and duration of antimicrobial therapy to maximize clinical cure or prevention of infection while limits the collateral damage of antimicrobial use, including toxicity, selection of pathogenic organism and emerge of resistance. Antimicrobial stewardship program helps the clinician to improve quality of care and patient safety through increase rate of infection cure, reduce treatment failure and increase appropriate prescribing.24
Large number of studies are conducted to assess the awareness & attitude of medical students on antibiotic resistance as well as stewardship, but few studies are there to measure the same in dental students.25-27 Keeping this lacuna in mind this study is initiated to assess the awareness and approach regarding antibiotic prescription in different level of dental students.
The cross-sectional study was conducted at Ziauddin University and teaching hospital; Karachi from 1st april, 2020 to 30th july,2020 and enrolled third and final year
dental students as well as house officers.28 Because firstand second-year dental students are not in clinical practice at this level, they were excluded from the study. After approved by the Institutional Ethics Committee of Ziauddin University, the sample size was calculated using Open Epi calculator. The computed sample size was 133 to which 5% non-response rate was added. Out of 139 students seventy- two were dental students and sixty- four were house officers. Non-probability convenience sampling technique was used.
All students in the study understood simple English, and, hence, it is selected as interview language in questionnaire. A self- designed, self-administered questionnaire29-32 was prepared to collect the demographic data and information regarding the prescription pattern of antibiotics amongst study subjects. All questions in the questionnaire were close ended. The questionnaire’s reliability was verified by calculating the alpha-coefficient, Cronbach’s which was found to be satisfactory. The questionnaire comprised information pertaining to Demographic characteristics, standard guideline for antibiotic prescriptions, antibiotic stewardship and resistance, improper prescription and its consequences. The questionnaire was filled by third and final year BDS students during class sessions by their teachers, to reduce information and selection bias. Data was obtained from house officers during their clinical rotations The dental students were briefed about the purpose of the study and the significance of participation and a written informed consent was obtained from them.
The data were analyzed by using SPSS version 22 and descriptive statistics were computed. The results were presented as means and standard deviations, frequencies,
and percentages. The R software version 3.1.1 (GNU General Public License) was used for computing. The frequency and percentage (percentage) of individuals who answered correctly for the various questions relating to socio-demographic variables, awareness regarding antibiotic usage were displayed using descriptive statistics. The Chi-square test of independence was used to evaluate the frequency of accurate responses across dental students and house officer.
The demographic data revealed that out of total 139 study participants,113(81.3%) were females, whereas 89(64%) of them were aged between 23-28 years. In our study 64(46%) of the participants were house officers. Moreover, only 18(12.9%) of them were in private practice (table 0).
of standard antibiotic prescribing guidelines most of the students were familiar (79.1%). Moreover, most students knew that amoxicillin is beta lactam antibiotic (87.8%).
Whereas half of the participants were aware that prolong use of antibiotics lead to superinfection. (54.7%); Least responses were received about antibiotic stewardship (17.3%). It was pleasingly seen that most of the participants are aware that antibiotics are not necessarily required in all dental infections (65.5%). Majority of dental students replied in favor of probability of Antibiotic abuse (92.1%). More than 2/3rd of the respondents believed that antibiotics aid in recovery of infections (84.9%). Their responses were positive towards antibiotic misuse leading to resistance (95%). While (77%) of the participants answered that they are aware that superinfection would be prevented by prescribing proper antibiotic dosage. Regarding, antibiotic stewardship ‘role in reducing its resistance, half of the participants were in favor (49.6%). Association of better efficacy of antibiotic with cost is denied by majority of participants (71.9%). While the majority believe that antibiotic should be continued even if symptoms are relieved. (64.7%). Almost equal dental students responded in favor (51.1%) and against (48.9%) of prescribing antibiotics without any senior consultation. It is encouraging to note that maximum dental students used to inquire recent antibiotic course prior to prescription (90.6%). Most of the respondents prefer to take extra precaution for prescribing antibiotic in immune compromised patients (89.9%). It is surprisingly seen that (23%) of the responders
experienced antibiotic resistance in their practice. While (10.8%) of the participants faced acute emergency due to antibiotic associated adverse effects (table 1).
Statistically a significant association between implementation of standard guidelines of antibiotic prescription with private clinical practices (p=0.011). In
addition, correlation of prolonged antibiotic use leads to super infection also significant with private clinical practice. (p value 0.001). A significant association (p value 0.023) is seen between resistance due to improper antibiotic therapy and gender. While experience of antibiotic resistance in clinical practice is significantly correlate with different level of qualification (p=0.002) (table 2).
Antibiotics have shown to be a powerful and effective arsenal against a variety of diseases during the previous five decades. Today, the development of antibiotic-resistant pathogenic bacteria and their dissemination in the human population is an increasing problem around the world, posing a serious threat to public health in the twenty-first century, especially in poor nations.33 Availability of antibiotic in Pakistan is as Over the counter (OTC). A study conducted in Pakistan supports this fact.34 An Indian study also revealed that (76%) of the Indian population purchase medicine from pharmacy based on their peer’ antibiotic experience prescribed by senior physician. This is in concordance to current study as this study revealed Almost equal dental students responded in favor (71%) and against (68%) of prescribing antibiotics without any senior consultation.
Another important issue is doctor mostly prescribe broad spectrum rather than narrow spectrum, even in scenarios where it is not needed, leading to antimicrobial resistance (AMR).35 It was pleasingly seen in present study that most of the participants were aware that antibiotics are not necessarily required in all dental infections (65.5%). In Pakistan, dentistry school lasts four years, and students in their second year of BDS complete a pharmacology course that covers prescription, pharmacology and pharmacokinetics knowledge. They begin to apply this knowledge throughout their clinical rotations in third, fourth year as well as during their house job. Dentists are free to work once they have completed their internship. In many investigations, dentists’ and dental students’ knowledge of drug prescription has been found to be insufficient.16 This shows that dental training should be enhanced throughout college years or while working as a house dentist. In order to train students and give them with the required ability to perform in a clinical setting, the medical curriculum should be well-rounded. There are gaps in the literature when it comes to evaluating
antibiotic prescription among dental students. One study compared the prescription patterns of dental students in their
last year and house officers.36 The goal of this study is to determine the level of awareness and approach to antibiotic prescription and resistance among dentistry students at various levels. In our research, we discovered that dental students had a good but not perfect understanding of several elements of antibiotics; similar findings have been reported in previous studies.29
The standard antibiotic prescribing guidelines were known by (79.1%) of the participants in our study. According to a survey done in India in 2017, (87.1%) of participants follow the rational prescription process. This could be related to dentistry school’s curriculum, which includes instruction on how to write rational prescriptions.28 Only (30%) of dental students followed WHO prescribing recommendations, according to Guzman’s research, while the remainder did not since most of them were uninformed of the guidelines.37 There was a significant correlation between the implementation of antibiotic guidelines and private practice in our research, indicating that they may have more autonomy in dealing with patients.
The results of this study revealed that (54.7%) were aware that superinfection has association with prolong antibiotic use while, a study conducted in India revealed that
(83.8%) medical students aware that superinfection is an adverse effect of prolong antibiotic use.38 In this study, we found that different levels of education were linked with the knowledge of superinfection associated with prolonged antibiotic usage. Another study revealed that higher education levels are certainly linked with better understanding.39 It’s encouraging to see that (90%) of the participants want to know about previous antibiotic courses before writing prescriptions. A study conducted in Lebanon in 2018 found that dentists follow a similar practice.40 (92.1%) of the participants believed that there is an abuse of antibiotic at present. Similar results have been showed by a study conducted in UAE.41 In our survey, 64.7 % said they would
finish their antibiotic course even if their symptoms improved, compared to 36.7 % who said they would quit taking antibiotics if their symptoms subside. On the contrary, according to a survey done in Lebanon, 48.5 % continue their antibiotic treatment even if their symptoms improve.42
In our study, antimicrobial misuse was mentioned as a source of antimicrobial resistance by (95%) of the participants. In 2017, Jamhour reported that (83%) of Lebanon’s 500
respondents were aware that antibiotic overuse can lead to microbial resistance.43 In 2020, Higuita-Gutiérrez and colleagues reported that medical students from three Medellin medical schools have low awareness of antibiotic use due to a lack of training in antibiotic use and bacterial resistance.44
In the same year, Veses and colleagues found that awareness programs are needed to promote student use of antibiotics in young generations, particularly among pre-professional health sciences students, after surveying undergraduate dental students at Universidad Cardenal Herrera.45 Due to lack of training, Tsopra in 2020 employed a game called ‘Anti-bio Game,’ in which students play the role of a doctor meeting patients in consultation, as a promising technique for
enhancing understanding in antibiotic prescription.46
Antibiotic resistance is a global public health problem and a potential threat to humanity, according to various stakeholders and health agencies, and there is utmost need
to combat this threat immediately.47 The majority of participants (90.6%) mentioned that knowing about antimicrobials and their appropriate use is crucial in their medical profession, indicating that future prescribers are concerned and aware of the extent and relevance of the issue. Aside from antibiotic prescribing, the ideas of developing antibiotic usage protocols in healthcare facilities should be taught as part of the undergraduate curriculum. Small group exercises that allow students to practice patient education skills, such as negotiating with patients about the need for antibiotics and educating them about effective antibiotic usage, should be a big element of the antibiotic curriculum for students. Only 17.3 % of the participants in our study responded about antibiotic stewardship. However, a study of medical and pharmacy students in East Africa found that pharmacy students had higher awareness of antibiotic stewardship. They believed their pharmacy degree program had covered antimicrobial stewardship concepts.48 According to these findings, the undergraduate medical/dental curriculum should include and emphasize antimicrobial stewardship and resistance principles from early years in order to enhance correct prescribing practice of future doctors. Further, policymakers should organize educational programs and workshops frequently to keep students up to date about antibiotic prescription and its associated resistance.
According to our findings, (89.9%) would take extra cautions while prescribing antibiotics for immunocompromised. Only patients in the high-risk category should be covered, according to new guidelines from the American Heart Association.49
There are certain limitations to our research. Recall bias could have influenced the responses. The students often do not practice what they tell. When the investigator is not there, their attitude may change. The outcome may not be applicable to the entire society. To validate the results on a broader population, a qualitative study should be conducted.Prescribing medication is a skill that doctors in practically every medical specialty need. Newly qualified doctors are typically exempt from having to begin high-risk practical procedures, they are frequently expected to prescribe powerful medications from the first day of clinical practice. To guide
their learning about future advancements, many graduates should require not only knowledge of today’s pharmaceuticals, but also a firm basis in therapeutic concepts, based by a scientific understanding of drug action.
This study concluded that Majority of the dental students had good awareness regarding antibiotics and factors related to it as participants responded positively to the 70% of awareness based questions.More than 2/3rd 79.1% responded they were familiar to standard antibiotic prescription guidelines, 87.8% responded Amoxicillin is beta lactam; for probability of Antibiotic abuse and antibiotics aid in recovery of infections majority showed awareness (92.1% and 84.9% respectively). 95% of them were aware about the improper use of Antibiotic and its associated resistance. 77% were in favor that super infection prevented by prescribing proper antibiotic dosage. Almost equal students inquire recent antibiotic course prior to prescription (90.6%) as well as take extra caution prescribing antibiotic in immune compromised patients (89.9%).
Our study gives the insight of awareness of antibiotic prescription among dental students, which guides the concerns to know the pattern and will help to narrow down the gap between academic knowledge and professional practice. Our study also stimulates the requirement for introduction of some strategies, for example, clinical case-based and problem-based learning from early years of undergraduate training with precise emphasis on the both short-and long-term perilous effects of illogical prescriptions of antimicrobials.
CONFLICT OF INTEREST
1. Jain A, Bhaskar DJ, Gupta D, Yadav P, Dalai DR, Jhingala V, Garg Y, Kalra M. Drug prescription awareness among the 3 rd year and final year dental students: A cross-sectional survey. J Indian Assoc Public Health Dent. 2015;13:73.
2. Iqbal A. The attitudes of dentists towards the prescription of antibiotics during endodontic treatment in north of Saudi Arabia. J Clin Diagn Res. 2015;9:ZC82.
3. He P, Sun Q, Shi L, Meng Q. Rational use of antibiotics in the context of China’s health system reform. Br Med J. 2019;365.
4. Kanneppady SS, Oo AM, Lwin OM, Al-Abed AA, Kanneppady SK. Knowledge, attitude, and awareness of antibiotic resistance among medical students. Archiv Medi Health Sci. 2019;7:57.
5. Aslam B, Wang W, Arshad MI, Khurshid M, Muzammil S, Rasool MH, Nisar MA, Alvi RF, Aslam MA, Qamar MU, Salamat MK. Antibiotic resistance: a rundown of a global crisis. Infect Drug Resis. 2018;11:1645.
6. Ramchurren K, Balakrishna Y, Mahomed S. Patients’ knowledge, attitudes and practices regarding antibiotic use at a regional hospital
in KwaZulu-Natal, South Africa 2017. Southern African J Infectious Dise. 2018;33:1-6.
7. Farley E, Stewart A, Davies MA, Govind M, Van den Bergh D, Boyles TH. Antibiotic use and resistance: Knowledge, attitudes and perceptions among primary care prescribers in South Africa. South Afr Medi J. 2018;108.
8. Roos NA, Bakar MA, Haque M. Knowledge, attitude and practice among Malaysian medical students, doctors, other health professionals and common people regarding antibiotic use, prescribing and resistance: A systematic review. Adv Human Biology. 2019;9:179.
9. Gandra S, Alvarez-Uria G, Turner P, Joshi J, Limmathurotsakul D, van Doorn HR. Antimicrobial resistance surveillance in low-and middle-income countries: progress and challenges in eight South Asian and Southeast Asian countries. Clin Microbiology Reviews. 2020;33:e00048-19.
10. Sarraf DP, Rai D, Rauniar GP. Knowledge, attitude and practices on antibiotic use and resistance among doctors in bp koirala institute
of health sciences. J Drug Deli Therapeut. 2018;8:170-5.
11. Hashemi S, Nasrollah A, Rajabi M. Irrational antibiotic prescribing: a local issue or global concern? EXCLI J. 2013;12:384.
12. Mboya EA, Sanga LA, Ngocho JS. Irrational use of antibiotics in the Moshi Municipality Northern Tanzania: a cross sectional study. Pan Afr Medi J. 2018;31.
13. Umar LW, Isah A, Musa S, Umar B. Prescribing pattern and antibiotic use for hospitalized children in a Northern Nigerian Teaching Hospital. Ann Afri Medi. 2018;17:26.
14. Koyuncuoglu CZ, Aydin M, Kirmizi NI, Aydin V, Aksoy M, Isli F, Akici A. Rational use of medicine in dentistry: do dentists prescribe
antibiotics in appropriate indications?. Eur J Clin Pharmacol. 2017;73:1027-32.
15. Teoh L, Stewart K, Marino R, McCullough M. Antibiotic resistance and relevance to general dental practice in Australia. Aus Dent J. 2018;63:414-21.
16. Ahsan S, Hydrie MZ, Hyder Naqvi SM, Shaikh MA, Shah MZ, Jafry SI. Antibiotic prescription patterns for treating dental infections in children among general and pediatric dentists in teaching institutions of Karachi, Pakistan. PloS one. 2020;15:e0235671
17. Amaha ND, Weldemariam DG, Abdu N, Tesfamariam EH. Prescribing practices using WHO prescribing indicators and factors associated with antibiotic prescribing in six community pharmacies in Asmara, Eritrea: a cross-sectional study. Antimicro Resist Infect Cont. 2019;8:1-7
18. Firouzabadi D, Mahmoudi L. Knowledge, attitude, and practice of health care workers towards antibiotic resistance and antimicrobial stewardship programmes: A cross-sectional study. J Evaluat Clin Pract. 2020;26:190-6.
19. Wong YC, Mohan M, Pau A. Dental students’ compliance with antibiotic prescribing guidelines for dental infections in children. J Indian Soci Pedodon Prevent Dent. 2016;34:348.
20. Global action plan on antimicrobial resistance;
21. Ghafur A, Mathai D, Muruganathan A, Jayalal JA, Kant R, Chaudhary D, Prabhash K, Abraham OC, Gopalakrishnan R, Ramasubramanian V, Shah SN. The Chennai Declaration: a roadmap to tackle the challenge of antimicrobial resistance. Indian J Cancer. 2013;50:71
22. De Vries TP, Henning RH, Hogerzeil HV, Fresle DA, Policy M, World Health Organization. Guide to good prescribing: a practical manual. World Health Organization; 1994.
23. Wasserman S, Potgieter S, Shoul E, Constant D, Stewart A, Mendelson M, Boyles TH. South African medical students’ perceptions and knowledge about antibiotic resistance and appropriate prescribing: are we providing adequate training to future prescribers?. South Afri Med J. 2017;107:405-10.
24. Ferdoush J, Parveen K, Ata M, Reza FH, Rahman MS. Knowledge, perception and preparedness of future prescribers about antimicrobial stewardship. Bangladesh J Pharmacol. 2016;11:928-34.
25. Shrestha R. Knowledge, attitude and practice on antibiotics use and its resistance among medical students in a tertiary care hospital. J Nepal Med Assoc. 2019;57(216):74.
26. Jairoun A, Hassan N, Ali A, Jairoun O, Shahwan M, Hassali M. University students’ knowledge, attitudes, and practice regarding antibiotic use and associated factors: a cross-sectional study in the United Arab Emirates. Int J General Medicine. 2019;12:235.
27. Shah S, Abbas G, Chauhdary Z, Aslam A, ur Rehman A, Khurram H, Noreen S, Chand UR, Younis MH, Zulfiqar U. Antibiotic use: A cross-sectional survey assessing the knowledge, attitudes, and practices amongst students of Punjab, Pakistan. J Am College Health. 2020:1-6.
28. Doshi A, Asawa K, Bhat N, Tak M, Dutta P, Bansal TK, Gupta R. Knowledge and practices of Indian dental students regarding the prescription of antibiotics and analgesics. Clujul Med. 2017;90:431.
29. Konde S, Jairam LS, Peethambar P, Noojady SR, Kumar NC. Antibiotic overusage and resistance: A cross-sectional survey among pediatric dentists. J Indian Soci Pedodont Prevent Dent. 2016;34:145.
30. Shaik T, Meher BR. A questionnaire based study to assess the knowledge, attitude and practice (KAP) of rationale use of antibiotics among undergraduate dental students in a tertiary care dental hospital of South India. Int J Basic Clin Pharmacol. 2017;6:312-5.
31. Jairoun A, Hassan N, Ali A, Jairoun O, Shahwan M. Knowledge, attitude and practice of antibiotic use among university students: a cross sectional study in UAE. BMC Public Health. 2019;19:1-8
32. Huang Y, Gu J, Zhang M, Ren Z, Yang W, Chen Y, Fu Y, Chen X, Cals JW, Zhang F. Knowledge, attitude and practice of antibiotics: a questionnaire study among 2500 Chinese students. BMC Med Educ. 2013;13:1-9.
33. Sakr S, Ghaddar A, Hamam B, Sheet I. Antibiotic use and resistance: An unprecedented assessment of university students’ knowledge, attitude and practices (KAP) in Lebanon. BMC Public Health. 2020;20:1-9.
34. Khan FU, Khan FU, Hayat K, Chang J, Saeed A, Khan Z, Ashraf M, Rasheed UM, Atif N, Ji W, Aziz MM. Knowledge, attitude and practices among consumers toward antibiotics use and antibiotic resistance in Swat, Khyber-Pakhtunkhwa, Pakistan. Expert review of anti-infective therapy. 2020;18:937-46.
35. Krockow EM, Colman AM, Chattoe-Brown E, Jenkins DR, Perera N, Mehtar S, Tarrant C. Balancing the risks to individual and society: a systematic review and synthesis of qualitative research on antibiotic prescribing behaviour in hospitals. J Hospital Infection. 2019;101:428-39.
36. Humayun A, Kadri W. A study comparing drug choices and prescription patterns amongst final year students and house officers in Karachi. Pak Oral Dent J. 2019;39:345-8.
37. Guzmán-Álvarez R, Medeiros M, Lagunes LR, Campos-Sepúlveda A. Knowledge of drug prescription in dentistry students. Drug Health Patient Saf. 2012;4:55-59.
38. Dawnji SR, Nair MK. Knowledge, attitude and practice of antibiotic use and resistance among second year medical students in a teaching hospital. J Med Sci Clin Res. 2018;6:198-203.
39. Vallin M, Polyzoi M, Marrone G, Rosales-Klintz S, Tegmark Wisell K, Stålsby Lundborg C. Knowledge and attitudes towards antibiotic use and resistance-a latent class analysis of a Swedish populationbased sample. PloS one. 2016;11:e0152160.
40. Mansour H, Feghali M, Saleh N, Zeitouny M. Knowledge, practice and attitudes regarding antibiotics use among Lebanese dentists. Pharmacy Practice (Granada). 2018;16(3).
41. Jairoun A, Hassan N, Ali A, Jairoun O, Shahwan M. Knowledge, attitude and practice of antibiotic use among university students: a cross sectional study in UAE. BMC Public Health. 2019;19:1-8.
42. Mouhieddine TH, Olleik Z, Itani MM, Kawtharani S, Nassar H, Hassoun R, et al. Assessing the Lebanese population for their knowledge, attitudes and practices of antibiotic usage. J Infect Public Health. 2015;8:20-31.
43. Jamhour A, El-Kheir A, Salameh P, Abi Hanna P, Mansour H. Antibiotic knowledge and self-medication practices in a developing country: a cross-sectional study. Am J Infect Control. 2017;45:384-8.
44. Higuita-Gutiérrez LF, Molina-Garcia V, Acevedo Guiral J, Gómez Cadena L, et al. Knowledge regarding antibiotic use among students of three medical schools in Medellin, Colombia: a cross-sectional study. BMC Med Educ. 2020;20:22.
45. Veses V, Del Mar J-SM, González-Martínez R, Cortell-Ballester I, Sheth CC. Raising awareness about microbial antibiotic resistance in undergraduate dental students: a research-based strategy for teaching non-laboratory elements of a microbiology curriculum. BMC Med Educ. 2020;20:47.
46. Tsopra R, Courtine M, Sedki K, Eap D, Cabal M, et al. AntibioGame®: a serious game for teaching medical students about antibiotic use. Int J Med Inform. 2020;136:104074.
47. Nadimpalli M, Delarocque-Astagneau E, Love DC, Price LB, Huynh BT, Collard JM, Lay KS, Borand L, Ndir A, Walsh TR, Guillemot D. Combating global antibiotic resistance: emerging one health concerns in lower-and middle-income countries. Clin Infect Diseases. 2018;66:963-9.
48. Lubwama M, Onyuka J, Ayazika KT, Ssetaba LJ, Siboko J, Daniel O, Mushi MF. Knowledge, attitudes, and perceptions about antibiotic use and antimicrobial resistance among final year undergraduate medical and pharmacy students at three universities in East Africa. Plos one. 2021;16:e0251301.
49. Suda KJ, Calip GS, Zhou J, Rowan S, Gross AE, Hershow RC, Perez RI, McGregor JC, Evans CT. Assessment of the appropriateness of antibiotic prescriptions for infection prophylaxis before dental procedures, 2011 to 2015. JAMA network open. 2019;2:e193909-.