|
 
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| REVIEW ARTICLE |
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| Year : 2019 | Volume
: 9
| Issue : 3 | Page : 179-183 |
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Knowledge, attitude and practice among Malaysian medical students, doctors, other health professionals and common people regarding antibiotic use, prescribing and resistance: A systematic review
Nur Aishah Che Roos, Muhamad Abu Bakar, Mainul Haque
Faculty of Medicine and Defence Health, Universiti Pertahanan Nasional Malaysia (National Defence University of Malaysia), Kuala Lumpur, Malaysia
| Date of Web Publication | 6-Sep-2019 |
Correspondence Address:
Mainul Haque
Unit of Pharmacology, Faculty of Medicine and Defence Health, Universiti Pertahanan National Malaysia (National Defence University of Malaysia), Kem Perdana Sungai Besi, 57000 Kuala Lumpur
Malaysia
 Source of Support: None, Conflict of Interest: None  | Check |
DOI: 10.4103/AIHB.AIHB_42_19
The use of antibiotics has been associated with the sizeable cutback of infectious disease mortality. Antibiotics also tremendously support the treatment of cancer, transplantation and many other surgeries. Currently, the development of new antibiotics has been slow down. Besides, there is a rapid process of antimicrobial resistance (AMR) against almost all available antibiotics. Moreover, there is quick progress of microbial development with multiple antibiotic resistant which adds more fatality. An independent search was performed from inception until January 2019 using electronic databases, including Medline, Scopus, Web of Science and PubMed for published articles. Seventeen articles were included; six among the medical professionals and students and 11 among the general public across the country. The quality of the included studies was deemed average. Medical, pharmacy and other university subjects' students' knowledge level were low to average. Often, medical and pharmacy students' knowledge level was better than others. One study clearly denoted that there is a gap between theoretical and practical input regarding antibiotic prescribing. Although medical officers and general physician knowledge level was good, but actual real-life attitude and practice cannot be assessed because of the study design. Common people had a lot of misunderstanding regarding antibiotic use and AMR. All these studies incorporated suggested that further educational intervention is warranted to promote prudent use of antibiotic and prevent AMR. This review similarly advocates educational interventions among all stakeholders of healthcare with a special emphasis on antibiotics stewardship and regulatory enforcement programme to promote rational use of antimicrobial and to prevent AMR.
Keywords: Antibiotic use, prescribing and resistance, common people, health professionals, knowledge, attitude, practice, Malaysia, systematic review
How to cite this article:
Che 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 Hum Biol 2019;9:179-83 |
How to cite this URL:
Che 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 Hum Biol [serial online] 2019 [cited 2023 Apr 1];9:179-83. Available from: https://www.aihbonline.com/text.asp?2019/9/3/179/266222 |
| Introduction | |  |
Globally, antimicrobial resistance (AMR) has been identified as the most high-profile danger for human health.[1] A recent report of the British Government estimated that around 700,000 people died every year because of AMR infections.[2] In addition, it was projected that the human extra casualty due to drug-resistant infection might rise to 10 million and the cost will increase to US$100 trillion internationally by another three decades.[3],[4],[5] Methicillin-resistant Staphylococcus aureus (MRSA) alone kills more US people each year (~19,000) than pulmonary emphysema, HIV/AIDS, Parkinson's disease and homicide combined.[6] Antimicrobials often prescribed without appropriate indication which has been blamed for triggering and promoting AMR. In the USA, it has been documented that every year, around 47 million prescriptions contain antibiotic irrationally and most of these prescriptions were for viral-originated common respiratory diseases that which do not demand antibiotics.[7] Antibiotics are mainly required for bacterial infections. In addition, Centers for Disease Control and Prevention assessed that <50% of these prescribed antibiotics for acute respiratory diseases were being irrational and imprudent.[8],[9],[10] This excessive use of antibiotics increases the possibility of adverse drug reactions and other complications, which include Clostridium difficile infectious diarrhoea.[11],[12] 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.[13],[14],[15],[16],[17]
A brief commentary on antibiotics uses in Malaysia
In Malaysia, antibiotics are one of the top utilised medicines for the treatment of respiratory tract infectious diseases.[18],[19] In addition, antibiotics were ranked first for healthcare cost and ninth for used quantities in 2008.[20] Antibiotics were more regularly prescribed in primary healthcare settings and mainly for respiratory infectious diseases.[19],[21],[22] Furthermore, antibiotics are often overprescribed in private healthcare facilities than that of public healthcare centres.[19] Another study revealed that antibiotic prescribing rates were high in both public and private primary healthcare centres in Malaysia, exclusively more observed in private settings. This study also exposed unnecessary and imprudent antibiotic utilisation for viral-originated infectious diseases. This study recommended educational approaches for all stakeholders to minimise the irrational use of antibiotics.[23] Another recent study reported that the irrational use of antibiotics was frequently observed in state-owned hospitals. Wrong selection of antibiotics was noticed around 40% of prescription. Although the National Antibiotic Guideline is regularly updated, on many occasion, researchers recognised that medical doctors have failed to comply with the recommended guidelines. Thereafter, a regular well-organised policy and a programme were advocated to improve antibiotic prescribing behaviour and prevent AMR.[24] Similar non-compliance of national guidelines was also found around 28 years back.[25] Subsequently, the objective of this manuscript is to systematically review the knowledge, attitude and practice (KAP) among Malaysian medical students, doctors, other health professionals and common people regarding antibiotic use, antibiotic prescribing and antibiotic resistance (ABR) to develop future policies and plans to combat microbial resistance and to ensure treatment success.
| Materials And Methods | | |
The reporting of this systematic review is in accordance with the preferred reporting items for systematic reviews and meta-analyses.[26]
Search strategy and selection criteria
An independent search was performed using electronic databases including Medline, Scopus, Web of Science and PubMed for articles published since inception till the 4th week of January 2019. The following keywords were used: (antibiotic(s) OR antimicrobial(s)) AND (resistance OR AMR) AND (knowledge OR attitude OR practice OR perception OR understanding) AND (medical doctor OR medical professional OR general practitioner OR physician OR medical student(s) OR medical undergraduate OR nurse(s) OR medical assistant(s)) for those in the medical field AND(public OR general OR student(s) OR parent(s) OR community) for the public. Cross-sectional studies (CSSs) investigating KAP on antibiotic use and ABR in medical personnel's and the people were considered. Studies conducted outside of Malaysia or focussed on antibiotics' prescription pattern and variability were excluded. No language restriction was applied.
Title and abstract of all retrieved articles were evaluated independently by two authors (NA and MH) against the inclusion and exclusion criteria. Articles that did not meet the eligibility criteria were excluded based on the study design, participants, exposure and outcome. Any disagreement was discussed and resolved by consensus.
Data extraction
Data from the selected studies were extracted independently by two reviewers (NA and MB) using a customised data extraction form. Any discrepancies in data extraction were discussed and resolved by consulting the third reviewer (MH). The following information was extracted from the eligible studies: (1) Study details (name of the first author, year of publication, article title); (2) study population (SP) for medical-related field or public, study setting, gender distribution; (3) survey characteristics (sampling method, sample size) and (4) study findings (response rate, survey outcomes, study limitation).
Quality assessment
The methodological quality of the included studies was assessed by two reviewers (NA and MH) using a modified Newcastle–Ottawa scale (NOS) adapted for CSSs.[27] The modified NOS uses the total number of stars to assess the quality of a survey. The following items were evaluated: (1) the representativeness of the sample and provision of power calculation, (2) characteristics of respondents and non-respondents, (3) ascertainment of exposure, (4) comparability of subjects in different groups and (5) appropriate statistical analyses. Studies scoring 9–10 stars were considered as high quality whereas studies scoring 7–8 stars were regarded as average quality. It has been discovered during the review process that populations and sampling methods were heterogeneous. Hence, meta-analysis was not performed.
Institutional approval
This study was approved by the Centre for Research and Innovation Management, Universiti Pertahanan Nasional Malaysia (National Defence University of Malaysia [NDUM]), Kem Sungai Besi, 57000 Kuala Lumpur, Malaysia, Code of Research: SF0052-UPNM/2018/SF/SKK/11, Memo No: UPNM (PPPI) 16/01/06 Jld 2 (31), dated December 14, 2018.
| Results | | |
Study selection
The process of searching and review of identified studies is depicted in [Figure 1]. A total of 561 citations (83 medical personnel and 478 public) were retrieved from the electronic databases using the defined keywords. Four records[28],[29],[30],[31] were identified from other sources including a general search on the internet, a review of the study references and study author. After removal of duplicates, 435 titles and abstracts were screened for eligibility. Four hundred and four records were excluded based on title and abstracts, geography and study design. Thirty-one full-texts were retrieved for detail examination of which only 17 studies were selected for inclusion in this review.[18],[28],[29],[30],[31],[32],[33],[34],[35],[36],[37],[38],[39],[40],[41],[42],[43] Reasons for excluding the remaining 14 studies include study design (animal study and database analysis), reports, duplicate publication, unpublished abstract, outcome studied focussing on drug dispensing and inaccessibility to the full-text article.
Methodological quality
Based on the study quality assessment tool used, only four of the included studies were considered good[30],[33],[34],[43] and seven studies were deemed to be average [Table 1].[29],[31],[37],[38],[39],[40],[42] The reporting of instrument–validation varies across studies. Six studies did not describe the steps taken to ensure the validity and reliability of the questionnaire used.[28],[31],[32],[35],[39],[41] Reliability coefficients assessed using the Cronbach's alpha were reported in nine studies.[28],[29],[30],[33],[39],[40],[41],[42],[43] Most studies have reported a reliability coefficient of ≥0.7, indicating acceptable internal consistency. All the included studies enrolled >100 participants. Two of the studies had a response rate of <50%[31],[37] while two studies did not report a response rate.[18],[35],[41] In ten studies,[18],[29],[30],[31],[33],[34],[35],[36],[40],[42] the convenience or universal sampling method was instigated which may subject the studies to a further selection bias. The main limitation identified from most studies is the generalisability of the findings due to the different region sampled across Malaysia.
Characteristics of selected studies
The components of the included studies are summarised in [Table 2]. Most studies were published after 2010 in Malaysia with the latest published in 2019. All studies enrolled participants aged 18 years or older, except in one study[18] in which the entry criteria include participants aged 16 years. In most of the reviews, over 50% of the participants enrolled are female. The study periods ranged from 2 to 18 months. | Table 2: Description of the studies regarding knowledge, attitude and use among Malaysian medical students, doctors, other health professionals and common people
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Six studies investigated those in the medical field in which all questionnaires were self-administered. Two studies assessed the knowledge of antibiotic prescribing and ABR among physicians.[37],[39] Tan et al. < sup>[39] have systematically sampled physicians based at the outpatient department of health clinics and hospital in Kedah, whereas Hassali et al.[37] enrolled physicians working in private practices around Selangor by employing the random sampling method. Three studies focussed on undergraduate medical and pharmacy students and have mostly used the universal sampling method. One study assessed the knowledge and attitude of 674 medical and non-medical students studying in the NDUM located in Kuala Lumpur.[30] In another study conducted at the (University Sultan Zainal Abidin) which is in the east coast of Malaysia,[40] only medical students in their clinical years were assessed for their knowledge on antibiotic prescribing and ABR. Meanwhile, Rajiah et al.[38] focussed on the understanding of ABR alone among final-year pharmacy students[38] enrolled in five public universities that were not specified in the text.
Seven studies explored the public residing in the northern region of Malaysia, including Penang[29],[33] and Perak[43] as well as Kuala Lumpur[18],[35],[42] and Putrajaya.[34] In addition to Kuala Lumpur, Islahudin et al.[35] also sampled population residing in the Kuantan district of Pahang. These studies assessed the knowledge, attitude, belief and/or practice of the public towards antibiotics used and ABR. All studies except one have employed the convenience sampling method. Choo et al.[43] have implemented the sequential sampling method whereby every fifth attendee at each study site (hospitals and health clinics) was approached to participate in their study. While the instrument was self-administered in most studies, Fatokun has conducted an interviewer-administered questionnaire on individuals residing in Cheras district.[18] Three studies[33],[34],[43] were based at hospitals or clinics while three other studies[29],[35],[42] were conducted in commercial centres such as the shopping complexes, supermarket, restaurants and residences. Fatokun[18] however did not describe their study setting in detail. In addition, four studies have explored the KAP towards antibiotics use among parents who are based in either Selangor or Kuala Lumpur.[28],[31],[32],[41] Three studies enrolled parents of children attending a clinic or hospital, and one study enrolled parents of children attending kindergartens in Kuala Lumpur.[31] In all the studies, over 50% of the participants were mothers.
Principal findings: Based on systematic review
Among the selected studies, four, one, one, three and seven were of medical and pharmacy students, medical officers, general practitioners (GPs), parents of children suffering from upper respiratory tract infections (URTIs) and common people with young adults, respectively, who assess KAP regarding antibiotic use and ABR.
Medical students
Two studies evaluated knowledge of antibiotics and resistance among medical students.[30],[40] It has observed that more than 50% of the medical students about antibiotic usage was knowledge level was low and their health beliefs were outdated. The same study tells the essentiality educational interventions which comprise education on the psychological aspects of prescribing antibiotics, health beliefs and patient expectations and an antibiotic stewardship programme to combat the irrational use of antibiotics and to help prevent AMR.[30] Another study clearly determined that there is a gap between theoretical input and clinical practice. Students have wanted more educational intervention to combat the potential threat of AMR. Clinical competency regarding antibiotic prescribing during their internship was principally learned by emulating senior colleagues, and this should be replaced by P-drug selection programme in the MBBS curriculum, throughout house-personship and refresher course all over practicing life.[40]
Pharmacy students
One study conducted among final-year pharmacy students revealed that moderately virtuous knowledge regarding antibiotic use and AMR. However, students' knowledge level did not correlate with attitudes. Most of the respondents did not possess a constructive attitude towards diminishing AMR. Mostly, students thought that educational intervention provides an essential feature in minimising AMR by promoting the prudent usage of antibiotics.[38] One more study reported that respondents had good knowledge level of AMR. Similarly, this study also concluded that an enhanced educational programme by altering the curriculum among all healthcare professionals, particularly physicians and pharmacists, can promote initiatives to fight against AMR. This study also advocated building appropriate professionalism in encouraging prudent use of antibiotics.[36]
Medical officers
Although medical officers possess average knowledge level, they prescribe antimicrobials frequently. Around two-thirds SPs were confident in antibiotic prescribing, but less than one-fifth had discussed among colleagues before prescribing antimicrobials. There was a significantly (P = 0.036) higher prescribing observed among junior doctors than seniors. In addition, there was also a significant association (P = 0.002) amidst rate of antibiotic prescribing and cognizance of AMR, among doctor's real-life practice.[39]
General physicians
Most of the GPs described that patients expect antibiotics. GPs (36.7%) apprehend that patients will demand from their physician if not prescribed antibiotics. However, more than one-fifth of the SPs clearly believe that antimicrobials were not needed and irrational utilisation to treat the case. This SP possesses a reasonable level of knowledge regarding prescribing for URTIs. However, the SP had apprehended that regarding subsequent antibiotic prescribing and patient pressure. This study finally concluded that there is an urgent need for educational interventions as an essential feature to combat against irrational use of antimicrobials and AMR among all stakeholders of healthcare which should include the patient community.[37]
Malaysian community other than health professionals
Parents of children suffering from upper respiratory infections
Parents frequently have low level of knowledge and misunderstandings regarding antibiotic for acute URTIs among children. Over 65% of the SP thought that antibiotics play an important role in treating the common cold, cough and fever, respectively. 29% of parents complained that although there was a need for antibiotic for their children for acute URTIs, doctors did not prescribe. Only 17% of SPs aware that antibiotics were not at all necessary for acute URTIs. Again, 28% of the SP demanded antibiotics for their children suffering from acute URTIs, and 93% were successful in obtaining antibiotic for children.[32] Another study reported that most of the parents have good knowledge level on antibiotic consumption. In addition, this SP had antibiotics for their children principally through medical doctors' prescription.[28] The majority (over 90%) of the SPs have experienced antibiotic before for their child, by doctor prescription, and follows the instructions of medical doctors. Nevertheless, more than one-third of them bought antibiotics from nearby medicine shop without a medical doctor's prescription. A good part of the study reported that only one-tenth of them had antibiotics for their child while suffering from influenza.[28] One more study revealed that in general, the SP had low-level knowledge nonetheless good attitudes regarding the usage of antibiotics in children with URTIs. Sex, educational level and monthly income were statistically significantly related to knowledge and attitude score level. This advocated that it is important to recognise the weak features of parental KAP. Thereafter, proper strategies can develop and executed to achieve better level KAP among parents and community to limit the irrational use of antibiotics.[31] Another study reported that most of the parent's knowledge regarding antibiotic use for URTIs was found low. However, more than about two-thirds of the parents were conscious of the AMR and AMR often promoted by excessive usage of antibiotics. Knowledge level was statistically significantly associated with parents' educational level and financial status. Solitarily mother's educational level was showed significantly related with the attitude. This study concluded that health promotional and educational movements are of extreme necessity to fight against imprudent use of antibiotics and AMR.[41]
Common people
Another study conducting among common people attending a hospital of Putrajaya, Malaysia, reported that there was a significant deficiency in knowledge and attitude level regarding appropriate antibiotics. Consequently, Malaysian patients and community are in danger of imprudent use of antibiotics and AMR. Both knowledge and attitude statistically significantly (P < 0.05) correlated with educational level, health-related occupation, gender, race and employment status. Around three-fourths of the SPs opined that they expect antibiotics for treatment of common colds and cough. Two-thirds of these study respondents accept as true that antibiotics speed up the recovery these ailments. This study finally concluded that educational interventions such as 'campaigns and patient counselling' among patients and community are essential to defending against imprudent use of antibiotics and AMR.[34] One more study conducted in major cities of Malaysia among common people found that more than two-thirds SP had antibiotics within the last 1 year more than one time. It was thought-provoking finding that those did not have antibiotic in the last year opined statistically significantly (P < 0.01) higher that AMR is a serious global public health threat for humanity. Those took antibiotic within the last 1 year did not take the full course of antibiotic. This study also similarly concluded that educational interventions among consumer and health professionals to develop appropriate knowledge and attitude in the direction of antibiotics consumption are essential to combat the irrational use of antibiotics and AMR.[35] One more cross-sectional study conducted among patients and attendants of Penang Hospital revealed that one-third of the SP possess a low level of knowledge and practice self-medication with antibiotics when suffering from common cold.[33] However, more than half of the SP had average knowledge regarding antibiotics. Nonetheless, more two-thirds of them believe that antibiotics are effective against viral diseases. In addition, just one-third of the respondents believe that antibiotic is indicated for the common cold and similar trivial diseases because of faster recovery from those ailments. On the contrary, more three-fourth of them clearly know that antibiotics are for bacterial infectious diseases. Again, more than half of the research respondents believe that AMR is strongly correlated with the irrational consumption of antibiotics. This study also found that educational level, age and ethnic origin were statistically significantly (P < 0.05) correlated with knowledge and attitude regarding antibiotic use. Consequently, this study also similarly concluded that educational interventions are the prime necessity among all stakeholders of healthcare to promote the rational use of antibiotics and prevent AMR.[33] Another cross-sectional study conducted in 13 hospitals and 44 primary healthcare centres of the state Perak among the adult population. The respondents were selected through the sequential sampling method who are educated and had experience with antibiotics. This study reported that most of the respondents expect antibiotics from medical doctors as a remedy for common trivial infection as antibiotic gear up the recovery process. Poor level of knowledge and attitude was found significant issues that contribute to promoting irrational use of antibiotic and AMR. In conclusion, this study also equally reported that the educational interventions are burning need with mass motivational campaign giving emphasis on prudent use of antibiotics and to prevent AMR.[43] One additional study among community dwellers in Pulau Pinang, Malaysia, reported that the SP had low level of knowledge and attitudes about antibiotic use and AMR.[29] Around four-fifth researches, respondents fail to recognise that antibiotic is only effective against bacterial infection. In addition, more three-fourth had confidence that antibiotics were effective medicine in treating influenza fever or similar diseases. Moreover, more than half of the research respondents had the notion that antibiotics are a complete healing agent for curing all infectious diseases. Furthermore, around three-fourths of them did not come to an agreement that resistant microorganism can spread both ways from 'human or animal to human.'[29] Despite the fact, nearing one-third of them were oblivious that microorganism had potential to develop resistance to antimicrobials. Moreover, around two-thirds of research population self-confessed that they took antibiotics when hospitalised to speed-up healing process from their ailment, and one-third of them stop antibiotics when started sensing improved.[29] This study again suggested well-designed 'community-based educational' programme, especially campaign to improve common people knowledge and attitude, and thereby combat imprudent use of antibiotics and to prevent AMR.[29] One more cross-sectional study conducting among the urban population on of Malaysia reported that four-fifths of the research respondents consumed antibiotics through medical doctors' prescription. Again, more than half of the research respondents suspend antibiotics when the disease process starts fading out. Respondents often dispose of leftover antibiotics in a bin with other garbage. This research also revealed with univariate analysis that sex (P = 0.04), poor knowledge level (P < 0.0001) regarding antibiotic use and insufficient, inadequate awareness (P < 0.0001) regarding potential threat of AMR to healthcare were the contributing factors for noncompliance to complete the full course of antibiotics. Again, this study also recommended education programme among patients about the atrocity AMR and prudent utilisation of antibiotics.[18]
Young Malaysia adults
Another cross-sectional study conducted in Kuala Lumpur, Malaysia, among young people. This SP was approached in a shopping centre, superstores, educational establishments, cafeterias and utility shops. The SP had a poor attitude regarding antibiotics consumption. Afterwards, documented a potential breach between attitude and practice among that research respondents. Nevertheless, more two-third research respondents approved that there is urgent to enhance educational intervention programme to enrich the knowledge level among community regarding antibiotic use and resistance. At last, this is the same way concluded educational interventions to improve antibiotic use and resistance. In addition, this study also recommended regulatory measures to control the easy availability of antibiotics over the counter.[42]
| Discussion | | |
AMR is escalating to precariously high levels in all areas of the globe, irrespective of developed and developing counties. AMR primarily increases healthcare costs, duration of hospitalisation, treatment failure and both morbidity and mortality.[44] AMR was the reason for 33,000 deaths every year in the European Union (EU) territory. Multidrug-resistant microbial infectious diseases in the EU increase healthcare costs around EUR 1.5 billion per year with a huge loss of work output.[45],[46] Another British Commission regarding microbial resistance reported that AMR could cause 10 million deaths a year by 2050.[47] Multiple studies revealed that currently, AMR accounts for enormous clinical and public health liability. These studies expect the threat to human healthcare because AMR will increase much more upcoming days. Thereafter, to address the burning of microbial resistance, certain programme and plan are necessary to enforce.[48],[49],[50],[51] This systematic review regarding the studies on the KAP of health professionals and common people on antibiotic use and resistance in Malaysia discusses the important elements to address the grave public health problem.
This review incorporated 17 original studies among Malaysian medical students.[18],[29],[30],[31],[32],[33],[34],[35],[36],[37],[38],[39],[40],[41],[42],[43],[44] These studies were CSSs. Accordingly, CSSs contain own inherent limitation. CSSs conducted at a certain point in time, as like a snapshot but not that of video or cinema.[52] Consequently, more suitable to evaluate the prevalence of variables of interest. CSSs also show recall bias.[53] Most importantly, CSSs cannot be utilised to appraise behaviour over a period to time, subsequently not suitable to appraise reason and outcome. Moreover, these types of studies possess probability with bias results as funding source can influence to obtain the desired outcome.[54],[55] Ultimately, these 17 studies had such limitations.[18],[29],[30],[31],[32],[33],[34],[35],[36],[37],[38],[39],[40],[41],[42],[43],[44] In daily English, the term attitude is typically used to mention an individual's feelings about a problem, thing or individual.[56] In addition, attitudes are interweaved with the individual's knowledge, beliefs, emotions and values, and it can be positive or negative.[57],[58] In KAP studies, the knowledge part is customarily utilised solitarily to evaluate the magnitude of individuals' or group of peoples' knowledge about public health perceptions associated to countrywide and worldwide public health programmes.[59] The second part of a typical KAP study assessing attitudes. Nevertheless, many KAP studies do not reveal results about attitudes. As there is a considerable hazard of misleadingly in generalising the thoughts of a precise cluster.[60],[61] Moreover, to assess medical students' attitude and practice regarding antibiotic use and resistance is a difficult procedure.
Medical students
Both the studies were conducted with a previously validated instrument.[62],[63] Those manuscripts were published in the highly reputed journal of this planet. The data collection instruments' quality was the basic strength of these two studies.[30],[40] Nevertheless, both studies had small SP study size and single-centre study. Thereafter, difficult to generalise the research result for the whole of the country. Researchers explained that these medical schools medical students intake were limited to only 50 students per year. Therefore, even universal sampling was adopted even then the sample size was small because the total SP was small. Both the studies equally recommended more educational inputs in undergraduate and postgraduate training period with the continued scholastic programme throughout the professional life to promoting prudent use of antibiotics and AMR.[30],[40]
Pharmacy students
The strength one study[39] was multi-center study. As five state-owned public university pharmacy students participated in the mentioned study. The questionnaire was developed very carefully depending on earlier published nine articles. The questionnaire was validated with Cronbach's alpha 0.82. The surveyed population was 346. The sample size was calculated based with a 5% margin of error, a 95% confidence level and a 50% response distribution. Thereafter, the appraised population was much higher than the calculated (201) sample. This study concluded that final-year pharmacy student had a good understanding regarding AMR, but most of the respondent did not possess a positive attitude in controlling and prevention of AMR.[38] The second study compared between medical (72) and pharmacy (51) students of International Islamic University of Malaysia.[36] The survey instrument was developed based on six earlier published articles. The questionnaire was pretested with the result of Cronbach's alpha 0.85. This study found a good understanding level in antibiotic use, AMR, mechanism of developing resistance in microbes and awareness towards minimising ABR.[36] There was no statistically significant difference observed between the two groups. Pharmacy students possess better understanding ability than medical students. This study did not claim the findings can be generalised because it was a single-centre study. Both the studies suggested enhanced educational programmes among all healthcare professionals, especially among physicians and pharmacists.[36],[38]
Medical officers
The study instrument was adopted from earlier two overseas studies.[64],[65] The instrument was initially developed in Peru[65] and again utilised in Congo.[64] Both the study published in very exceedingly reputed journals. The survey instrument was appraised again by public health physician to assess its applicability for local Malaysian context.[39] The instrument was validated through a pilot study. The validation score was not described in the study. The sample size was calculated with the formula described in another study.[66] The sample was 118 with presumed 20% non-respondents.[39] This study concluded that Malaysian medical officers possess a reasonable level of knowledge regarding antibiotic. There was no statistically significant (P = 0.72) differences observed between senior and junior medical officers in knowledge level. Most of the research respondents were confident in prescribing, and most of them never consult among them to select and prescribe antibiotics. Again, the majority of medical officers prescribe antibiotics daily. In addition, there were statistically (P < 0.05) significant differences observed senior and junior medical officers and frequency of antibiotic prescribing and awareness of AMR in their daily practice. The strength of this study was the compassion between senior and juniors and comparison awareness level and prescribing. These study findings were quite like earlier one systematic review.[67]
General physicians
The study instruments were developed based on the previously published article.[68] GPs were only selected from one state, although Malaysia is a federation consisting of 13 states and three federal territories.[37] The sample size web-based system with a confidence limit of 95%, an error margin of 5% and a prevalence of 50%. The calculated sample size was 303% + 30% nonresponse rate; it was 400.[37] The calculation of the sample size was one of the strengths of the study. This research also disclosed that about low response rate, there might be a possible difference between respondents and non-respondents. As because of KAP study, it may have a biased result as respondents answered carefully so that can avoid societal conflict. However, 81.3% of the SP had moderate-to-good level of knowledge regarding antibiotic prescribing for URTIs. Nevertheless, 84.93% of studied general physicians prescribed antibiotics for running nose, sore throat and otitis media. Moreover, 89.2% thought that AMR is a major public health problem.[37] Regarding medical officers[39] and general physicians,[37] studies revealed that actual evaluation of prescribing practice was not possible because of CSS and KAP study.
Malaysian community other than health professionals
Parents of children suffering from upper respiratory infections
This study instrument how was developed or adopted was not described.[32] The sampling method was universal, and the sample size was 421. The study respondents were incorporated from publicly owned primary healthcare centres, Cheras Mukim of Hulu Langat district, Malaysia. The study did not describe how researchers ensure how all parents were incorporated as the study respondents. Parents' knowledge regarding antibiotic use was inadequate. Majority of the parents believe antibiotics are helpful for URTIs and demanded antibiotics for their children.[32] Another similar study incorporated respondents from children clinic of Hospital Serdang, Malaysia.[28] Respondents were parents of those children visited for treatment in the mentioned health centre. This study instrument was pre-tested before, but pre-tested results were not described. In addition, how the instrument was developed did not also describe. The sample size how calculated was not pronounced. The sampling method was random. The SP was 229, but again what was the total population was not mentioned. The respondents of this study good knowledge and practice regarding antibiotic use.[28] One additional study conducted among parents of kindergarten children of Kuala Lumpur, Malaysia.[31] The study instrument was adopted from an earlier study with the expectation it will best suit the local context.[69] This study did not describe embraced instrument whether validated for the local context. Moreover, the sampling method and sample size how calculated were not described. This study found that two-thirds of the SP knowledge level were a poor but largely positive attitude. There was a statistically significant (P < 0.05) relationship between knowledge and attitude, and a moderate negative correlation (rs = −0.498) exists between knowledge and attitude. This study finally concludes that although the SP possesses poor knowledge in parallel, SP holds positive attitudes about the use of antibiotics. This study principal strength was the statistical part.[31] One more study selected for the current review conducted among 320 parents attending in the primary healthcare centre, situated in Bandar Tasik Selatan, Kuala Lumpur, Malaysia.[41] The questionnaire was adopted from the overseas earlier published study.[70] Researchers translated in the questionnaire in the local language and conducted pre-test for validation of the instrument. The pre-test scores were Cronbach's alpha of 0.626 for knowledge and 0.769 for attitude. This validation was the strength of the study. Nevertheless, this research did not how sample size and sample method. The sample size was 320. Most of the SP poor knowledge level regarding antibiotic.[41] Although the study detected most of the respondents had a good attitude regarding usage, most of the parents preferred antibiotics for their children when suffered from URTIs. At least one-third respondents express their desire for antibiotics for children. This study revealed statistically significant (P < 0.05) association with knowledge and parental (fathers: [OR] = 2.79, 95% confidence interval [CI] 1.620–4.800, P < 0.001; mothers: OR = 2.36, 95%CI 1.376–4.035, P = 0.002) education level and family income. Nonetheless, mother's educational level was significantly associated with their attitude level (OR = 2.19, 95% CI 1.121–4.267, P = 0.020). In addition, there was a statistically significant (P < 0.05) association between this practice with the gender of the respondents, father's educational level, mother's educational level and family income. The best part of this study was statistical analysis.[41]
Common people
One study conducted among people attending in a local hospital of Putrajaya, Malaysia.[34] The study instrument was developed based on five published articles. Initially, the instrument was developed in English and then translated in Malay. Face and content validation of the questionnaire were examined by senior staffs of the institute. The instrument was pre-tested, and test results were Cronbach's alpha 0.68–0.74. The sample size was calculated with the web-based system. Researchers depend on convenience sampling method. This study analyses the data by utilising t-test, ANOVA, multiple logistic regressions with the adjusted ORs and Pearson's correlation and Chi-square test. In all statistical analyses, a P < 0.05 was considered statistically significant.[34] Highest education level and healthcare-related occupation were statistically significantly (P < 0.05) related to knowledge score, whereas gender, race, highest education level, employment status and healthcare-related occupation were statistically significantly (P < 0.05) associated with attitude score.[34] Like earlier few studies, the principal strength was a statistical portion.[34] Another study conducted common people of Kuantan and Kuala Lumpur, Malaysia.[35] The study respondents incorporated conveniently from shopping malls of these metropolises. This study did not describe how the study instrument was developed, what the sampling method was and how the sample size was calculated. Although this study did not find any statistically significant correlation among knowledge and antibiotics usage, but statistically significant association detected with antibiotic usage and attitude, similarly with practice.[35] This study did not mention P value and statistical test name. The analytical part of this research was not adequately described.[35] One more study among common people which include patients and other hospital attendees of the Outpatient Pharmacy Department of Penang Hospital, Malaysia.[33] The study instrument was developed depending on four earlier published studies. The instrument was developed initially in English and then translated to Malay. Face and content validation were conducted by the senior members of the faculty. The instrument was validated for local context by doing pre-test and score was Cronbach's alpha was 0.76. The statistical test was Chi-square and Fisher's exact tests. Most of the respondents' overall knowledge was at a good level, but nonetheless, they opined that antibiotic is indicated and effective in viral diseases. There was statistically significant (P < 0.05) relationship exist between knowledge and age group, race, educational status and monthly income. This study also revealed a weak positive correlation (r = 0.276, N = 408, P < 0.001) between knowledge and attitude. Overall both methods and data analysis strength were good of those research were incorporated in this systematic review.[33] Another study was conducted among common people. The study respondents were incorporated as came as an attendant of patients of 13 hospitals and 44 primary health clinics in Perak, Malaysia, who are 18 years and above, well-read and had experience in antibiotics usage. The sample size was calculated with software namely EpiCalc: Epidemiological calculator. Again, the sequential sampling method was adopted for this study. The study instrument was developed based on four earlier published articles. The instrument was in initially developed in the English language and then translated in Malay. The face and content validation were done by the senior academicians of those hospitals. A pre-test was carried out, and the scores of Cronbach's alphas were above 0.7. The statistical analysis was with explored using t-test, ANOVA and Chi-square test. The level of statistical significance was set at P < 0.05.[43] The study respondents' age, sex, uppermost educational level, healthcare linked profession and knowledge on ABR had statistically significant (P < 0.05) association with mean belief, knowledge and practice. Finally, of all, the ethnic origin of the respondents also associated with knowledge score (P = 0.002). This study quality regarding methods and statistical part was good enough.[43] One more study conducted among 326 peoples of the Jelutong district, Pulau Pinang state, Malaysia. The instrument was developed based on earlier published three studies. The SP was incorporated through the conveniencesampling method. Nevertheless, how sample size was calculated was not described in the manuscript. As like other studies initially, the instrument was developed in English and then translated in Malay by a specialised translator as per described by the United States Census Bureau.[71] The face and content validation of the instrument was completed by senior academicians of Universiti Sains Malaysia. Researchers performed a pilot study to assess the reliability and the score of Cronbach's alpha was 0.647.[43] This only describes results only in percentage (%); no other statistical test was described. Although this study method was good, analysis can be more extended to compare among the groups.[43] One more study was performed in Cheras, a municipal situated to the south-east of Kuala Lumpur, Malaysia.[18] The questionnaire was settled from earlier published three studies, and convenience sampling was adopted for data uptake which was face-to-face questionnaire-based interview. Researchers performed a pilot study for validation of the instrument nonetheless did not describe the pilot study result.[18] The study analysed the data by doing a descriptive analysis with univariate analysis utilising a Chi-square test. This study revealed that more than half of the respondents were aware of AMR. 49.6%, 55.2%, 89.2%, 80%, 73.2% and 78.8% of the study respondents opined that they completed the course of antibiotics, usually discontinued when symptoms start died out, obtained antibiotics from hospital or clinic, they were on no occasion obtained antibiotics without doctors' prescription, they were not ever saved excess antibiotics and surplus antibiotics disposes in household bin.[18] This study also found statistically significant (P < 0.05) higher noncompliance among male research respondents than their female counterpart. Poor knowledge level and not aware about AMR also obsereved. Nonetheless, age, ethnicity, marital status and antibiotic acquisition were not statistically significantly (P > 0.05) related to antibiotic compliance.[18] This study method, analysis and result section can be considered above average.
Young adults
This systematic review includes only one study where the SP was young Malaysian adults. The SP was conscripted from Cheras, located in the southeast of the Federal Territory of Kuala Lumpur, Malaysia.[42] The sample size was calculated using Krejcie, and Morgan's sample size calculator and a convenience sampling method were used to recruit 480 SP. The study instrument was developed based on six published earlier studies. The drafted questionnaire content validity was examined by two scholastic persons of medical and pharmacy upbringing with profound experience in transmittable disease and survey-based study. The final version of the instrument was subject to a pilot test, and Cronbach's alpha was 0.745. This study utilised logistic regression analysis and P < 0.05 was statistically significant.[42] This study revealed that ethnicity plays a role to promote a positive attitude towards antibiotics usage (OR = 1.836, P < 0.05). In addition, participants with higher education exhibited positive attitudes (OR = 1.689, P < 0.05). Again, the attitude of healthcare workers was better than others (OR = 1.806, P < 0.05). High income of the participants also appeared to be a significant predictor of their attitude (OR = 2.071, P < 0.05). The practices of female SP were better (OR = 1.934, P < 0.05). Similarly, Chinese participants had good practices than other ethnic groups of this study (OR = 3.309, P < 0.05). Income of the participants also appeared to be a significant predictor of their practice. The SP with better monthly income better practices (OR = 2.498, P < 0.05).[42] This study both methods, statistical analysis and result section were good enough.
Overall, all these studies incorporated in this systematic review had ethical approval. All these finally recommended more educational intervention to promote prudent use of antimicrobials and prevention of AMR. The similar recommendation also suggested by several recent research.[72],[73],[74],[75] Several studies demanded strict regulatory policies and planning to promote rational utilisation of antimicrobials and prevent AMR, especially need to enforce to stop over the counter sale of antimicrobials.[76],[77],[78],[79]
| Conclusion | | |
Almost all studies incorporated in this systematic review agreed that in Malaysia there were imprudent use of antibiotics, microbial resistance with MDR exist in this country which is a significant public health issue. There is an urgent need for educational intervention with mass communication for ordinary people to develop better awareness level regarding antibiotic use. Similarly, an educational intervention like regular refresher courses is essential for health professionals including medical doctors, general physicians and consultants for improvement more prudent use antibiotics. Moreover, medical students need more practical emphasis on clinical pharmacology. Beside that there is urgent need to develop strategies to prevent over-the-counter sell of antibiotics. Regulatory bodies must ensure that pharmacy shops must not sell antimicrobials without a prescription of Malaysian Medicals Council registered medical practioner. Antimicrobial stewardship programme accentuates purposeful, correct antimicrobial management scheme for the advantage of the individual patient and community. Therefore, in Malaysia, there is an imperative necessity for antimicrobial stewardship programme which will protect remaining antimicrobials for forthcoming days to ensure treatment success.
Acknowledgement
We are much appreciative to the library authority of NDUM, Kem Perdana Sungai Besi, 57000 Kuala Lumpur, Malaysia, for providing all necessary articles for this paper.
Financial support and sponsorship
Nil.
Conflicts of interest
There are no conflicts of interest.
| References | | |
| 1. | Llor C, Bjerrum L. Antimicrobial resistance: Risk associated with antibiotic overuse and initiatives to reduce the problem. Ther Adv Drug Saf 2014;5:229-41.  |
| 2. | O'Neill J. Tackling Drug-Resistant Infections Globally: Final Report and Recommendations 2016. The UK Prime Minister Commissioned the Review on Antimicrobial Resistance to Address the Growing Global Problem of Drug-Resistant Infections. Supported by the Wellcome Trust and UK Government, but Operates AND Speaks with Full Independence from Both. Available from: https://amr-review.org/sites/default/files/160518_Final%20paper_with%20cover.pdf. [Last accessed on 2019 Jan 26]. |
| 3. | Jasovský D, Littmann J, Zorzet A, Cars O. Antimicrobial resistance-a threat to the world's sustainable development. Ups J Med Sci 2016;121:159-64. |
| 4. | Shallcross LJ, Howard SJ, Fowler T, Davies SC. Tackling the threat of antimicrobial resistance: From policy to sustainable action. Philos Trans R Soc Lond B Biol Sci 2015;370:20140082. |
| 5. | |
| 6. | Infectious Diseases Society of America (IDSA), Spellberg B, Blaser M, Guidos RJ, Boucher HW, Bradley JS, et al. Combating antimicrobial resistance: Policy recommendations to save lives. Clin Infect Dis 2011;52 Suppl 5:S397-428. |
| 7. | Fleming-Dutra KE, Hersh AL, Shapiro DJ, Bartoces M, Enns EA, File TM Jr., et al. Prevalence of inappropriate antibiotic prescriptions among US ambulatory care visits, 2010-2011. JAMA 2016;315:1864-73. |
| 8. | Centers for Disease Control and Prevention (CDC). Office-related antibiotic prescribing for persons aged ≤14 years – United States, 1993-1994 to 2007-2008. MMWR Morb Mortal Wkly Rep 2011;60:1153-6. |
| 9. | Shapiro DJ, Hicks LA, Pavia AT, Hersh AL. Antibiotic prescribing for adults in ambulatory care in the USA, 2007-09. J Antimicrob Chemother 2014;69:234-40. |
| 10. | Gonzales R, Malone DC, Maselli JH, Sande MA. Excessive antibiotic use for acute respiratory infections in the United States. Clin Infect Dis 2001;33:757-62. |
| 11. | Peng Z, Ling L, Stratton CW, Li C, Polage CR, Wu B, et al. Advances in the diagnosis and treatment of Clostridium difficile infections. Emerg Microbes Infect 2018;7:15. |
| 12. | Fordtran JS. Colitis due to Clostridium difficile toxins: Underdiagnosed, highly virulent, and nosocomial. Proc (Bayl Univ Med Cent) 2006;19:3-12. |
| 13. | Centers for Disease Control and Prevention (CDC). Vital signs: Preventing Clostridium difficile infections. MMWR Morb Mortal Wkly Rep 2012;61:157-62. |
| 14. | Dantes R, Mu Y, Hicks LA, Cohen J, Bamberg W, Beldavs ZG, et al. Association between outpatient antibiotic prescribing practices and community-associated Clostridium difficile infection. Open Forum Infect Dis 2015;2:ofv113. |
| 15. | Kutty PK, Benoit SR, Woods CW, Sena AC, Naggie S, Frederick J, et al. Assessment of Clostridium difficile-associated disease surveillance definitions, North Carolina, 2005. Infect Control Hosp Epidemiol 2008;29:197-202. |
| 16. | Lessa FC, Mu Y, Bamberg WM, Beldavs ZG, Dumyati GK, Dunn JR, et al. Burden of Clostridium difficile infection in the United States. N Engl J Med 2015;372:825-34. |
| 17. | Peery AF, Dellon ES, Lund J, Crockett SD, McGowan CE, Bulsiewicz WJ, et al. Burden of gastrointestinal disease in the United States: 2012 update. Gastroenterology 2012;143:1179-87.e3. |
| 18. | Fatokun O. Exploring antibiotic use and practices in a Malaysian community. Int J Clin Pharm 2014;36:564-9. |
| 19. | Teng CL, Tong SF, Khoo EM, Lee V, Zailinawati AH, Mimi O, et al. Antibiotics for URTI and UTI – Prescribing in Malaysian primary care settings. Aust Fam Physician 2011;40:325-9. |
| 20. | |
| 21. | Teng CL, Nik-Sherina H, Ng CJ, Chia YC, Atiya AS. Antibiotic prescribing for childhood febrile illness by primary care doctors in Malaysia. J Paediatr Child Health 2006;42:612-7. |
| 22. | Mohd Fozi K, Kamaliah M. The effect of profiling report on antibiotic prescription for upper respiratory tract infection. Malays Fam Physician 2013;8:26-31. |
| 23. | Ab Rahman N, Teng CL, Sivasampu S. Antibiotic prescribing in public and private practice: A cross-sectional study in primary care clinics in Malaysia. BMC Infect Dis 2016;16:208. |
| 24. | Hong Tan GH, Low QW, Lim HC, Seah HK, Chan HK. Inappropriate antibiotic utilization: Outpatient prescription review of a regional secondary hospital in Kedah, Malaysia. J Pharm Pract Community Med 2017;3:215-9. |
| 25. | Lim VK, Cheong YM, Suleiman AB. Pattern of antibiotic usage in hospitals in Malaysia. Singapore Med J 1993;34:525-8. |
| 26. | Liberati A, Altman DG, Tetzlaff J, Mulrow C, Gøtzsche PC, Ioannidis JP, et al. The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate health care interventions: Explanation and elaboration. PLoS Med 2009;6:e1000100. |
| 27. | Modesti PA, Reboldi G, Cappuccio FP, Agyemang C, Remuzzi G, Rapi S, et al. Panethnic differences in blood pressure in Europe: A systematic review and meta-analysis. PLoS One 2016;11:e0147601. |
| 28. | Darussalam SE, Tompell AB, Juni MH, Abidin MA. A cross-sectional study to assess knowledge and practice regarding antibiotic used among parents of children attending pediatric clinic. Int J Public Health Clin Sci 2017;4:172-81. |
| 29. | Halim NA, Chang CT, Chan HK, Hassali MA, Nouri A. Knowledge and attitudes concerning antibiotic use and resistance among the public in Pulau Pinang, Malaysia. Malays J Med Sci 2018;25:141-7. |
| 30. | Haque M, Rahman NA, McKimm J, Binti Abdullah SL, Islam MZ, Zulkifli Z, et al. Across-sectional study evaluating the knowledge and beliefs about, and the use of antibiotics amongst Malaysian University students. Expert Rev Anti Infect Ther 2019;17:275-84. |
| 31. | Shah NM, Rahim MA. Parental knowledge, attitudes, and practices (KAPs) on the use of antibiotics in children for upper respiratory tract infections (URTIs). Int J Pharm Pharm Sci 2017;9:105-10. |
| 32. | Chan GC, Tang SF. Parental knowledge, attitudes and antibiotic use for acute upper respiratory tract infection in children attending a primary healthcare clinic in Malaysia. Singapore Med J 2006;47:266-70. |
| 33. | Ling Oh A, Hassali MA, Al-Haddad MS, Syed Sulaiman SA, Shafie AA, Awaisu A. Public knowledge and attitudes towards antibiotic usage: A cross-sectional study among the general public in the state of Penang, Malaysia. J Infect Dev Ctries 2011;5:338-47. |
| 34. | Lim KK, Teh CC. A cross sectional study of public knowledge and attitude towards antibiotics in Putrajaya, Malaysia. South Med Rev 2012;5:26-33. |
| 35. | Islahudin F, Tamezi AM, Shah NM. Knowledge, attitudes and practices about antibiotic use among the general public in Malaysia. Southeast Asian J Trop Med Public Health 2014;45:1474-82. |
| 36. | Jamshed SQ, Elkalmi R, Rajiah K, Al-Shami AK, Shamsudin SH, Siddiqui MJ, et al. Understanding of antibiotic use and resistance among final-year pharmacy and medical students: A pilot study. J Infect Dev Ctries 2014;8:780-5. |
| 37. | Hassali MA, Kamil TK, Md Yusof FA, Alrasheedy AA, Yusoff ZM, Saleem F, et al. General practitioners' knowledge, attitude and prescribing of antibiotics for upper respiratory tract infections in Selangor, Malaysia: Findings and implications. Expert Rev Anti Infect Ther 2015;13:511-20. |
| 38. | Rajiah K, Ren WS, Jamshed SQ. Evaluation of the understanding of antibiotic resistance among Malaysian pharmacy students at public universities: An exploratory study. J Infect Public Health 2015;8:266-73. |
| 39. | Tan WL, Siti R, Shahfini I, Zuraidah A. Knowledge, attitude and practice of antibiotics prescribing among medical officers of public health care facilities in the state of Kedah, Malaysia. Med J Malaysia 2015;70:307-11. |
| 40. | Haque M, Rahman NI, Zulkifli Z, Ismail S. Antibiotic prescribing and resistance: Knowledge level of medical students of clinical years of University Sultan Zainal Abidin, Malaysia. Ther Clin Risk Manag 2016;12:413-26. |
| 41. | Teck KC, Ghazi HF, Bin Ahmad MI, Binti Abdul Samad N, Ee Yu KL, Binti Ismail NF, et al. Knowledge, attitude, and practice of parents regarding antibiotic usage in treating children's upper respiratory tract infection at primary health clinic in Kuala Lumpur, Malaysia: Pilot study. Health Serv Res Manag Epidemiol 2016;3:2333392816643720. |
| 42. | Hassali MA, Arief M, Saleem F, Khan MU, Ahmad A, Mariam W, et al. Assessment of attitudes and practices of young Malaysian adults about antibiotics use: A cross-sectional study. Pharm Pract (Granada) 2017;15:929. |
| 43. | Choo SJ, Chang CT, Lee JC, Munisamy V, Tan CK, Raj JD, et al. A cross-sectional study on public belief, knowledge, and practice towards antibiotic use in the state of Perak, Malaysia. J Infect Dev Ctries 2018;12:960-9. |
| 44. | Tang Q, Song P, Li J, Kong F, Sun L, Xu L. Control of antibiotic resistance in china must not be delayed: The current state of resistance and policy suggestions for the government, medical facilities, and patients. Biosci Trends 2016;10:1-6. |
| 45. | |
| 46. | |
| 47. | |
| 48. | de Kraker ME, Davey PG, Grundmann H; BURDEN study group. Mortality and hospital stay associated with resistant Staphylococcus aureus and Escherichia coli bacteremia: Estimating the burden of antibiotic resistance in Europe. PLoS Med 2011;8:e1001104. |
| 49. | Stewardson AJ, Allignol A, Beyersmann J, Graves N, Schumacher M, Meyer R, et al. The health and economic burden of bloodstream infections caused by antimicrobial-susceptible and non-susceptible Enterobacteriaceae and Staphylococcus aureus in European hospitals, 2010 and 2011: A multicentre retrospective cohort study. Euro Surveill 2016;21:303-19. |
| 50. | de Kraker ME, Wolkewitz M, Davey PG, Koller W, Berger J, Nagler J, et al. Clinical impact of antimicrobial resistance in European hospitals: Excess mortality and length of hospital stay related to methicillin-resistant Staphylococcus aureus bloodstream infections. Antimicrob Agents Chemother 2011;55:1598-605. |
| 51. | Stewardson A, Fankhauser C, De Angelis G, Rohner P, Safran E, Schrenzel J, et al. Burden of bloodstream infection caused by extended-spectrum β-lactamase-producing Enterobacteriaceae determined using multistate modeling at a Swiss University hospital and a nationwide predictive model. Infect Control Hosp Epidemiol 2013;34:133-43. |
| 52. | Setia MS. Methodology series module 3: Cross-sectional studies. Indian J Dermatol 2016;61:261-4. [ PUBMED] [Full text] |
| 53. | Laake P, Benestad HB, Olsen BR. Research in Medical and Biological Sciences. 2 nd ed. London Wall: Academic Press; 2015. |
| 54. | Simundić AM. Bias in research. Biochem Med (Zagreb) 2013;23:12-5. |
| 55. | Tripepi G, Jager KJ, Dekker FW, Wanner C, Zoccali C. Bias in clinical research. Kidney Int 2008;73:148-53. |
| 56. | Petty RE, Cacioppo JT. Attitudes and Persuasion-Classic and Contemporary Approaches. Third Avenue, New York, USA, Routledge, Taylor & Francis Group; 2018. p. 6-7. |
| 57. | Fang WT, Eric Ng E, Wang CM, Hsu ML. Normative beliefs, attitudes, and social norms: People reduce waste as an index of social relationships when spending leisure time. Sustainability 2017;9:1696. |
| 58. | Howe LC, Krosnick JA. Attitude strength. Annu Rev Psychol 2017;68:327-51. |
| 59. | Launiala A. How much can a KAP survey tell us about people's knowledge, attitudes, and practices? Some observations from medical anthropology research on malaria in pregnancy in Malawi. Anthropol Matters J 2009;11:1-13. |
| 60. | Cleland J. A critique of KAP studies and some suggestions for their improvement. Stud Fam Plann 1973;4:42-7. |
| 61. | Hausmann-Muela S, Muela RJ, Nyamongo I. Health-Seeking Behavior and the Health System's Response. DCPP Working Paper no 14; 2003. Available from: http://dcp2.org/file/29/wp14.pdf. [Last accessed on 2019 Mar 27]. |
| 62. | Dyar OJ, Pulcini C, Howard P, Nathwani D; ESGAP (ESCMID Study Group for Antibiotic Policies). European medical students: A first multicentre study of knowledge, attitudes and perceptions of antibiotic prescribing and antibiotic resistance. J Antimicrob Chemother 2014;69:842-6. |
| 63. | Awad AI, Aboud EA. Knowledge, attitude and practice towards antibiotic use among the public in Kuwait. PLoS One 2015;10:e0117910. |
| 64. | Thriemer K, Katuala Y, Batoko B, Alworonga JP, Devlieger H, Van Geet C, et al. Antibiotic prescribing in DR Congo: A knowledge, attitude and practice survey among medical doctors and students. PLoS One 2013;8:e55495. |
| 65. | García C, Llamocca LP, García K, Jiménez A, Samalvides F, Gotuzzo E, et al. Knowledge, attitudes and practice survey about antimicrobial resistance and prescribing among physicians in a hospital setting in Lima, Peru. BMC Clin Pharmacol 2011;11:18. |
| 66. | Naing L, Winn T, Rusli BN. Practical issues in calculating the sample size for the prevalence studies. Arch Orofac Sci 2006;1:9-14. |
| 67. | Chaw PS, Höpner J, Mikolajczyk R. The knowledge, attitude and practice of health practitioners towards antibiotic prescribing and resistance in developing countries-A systematic review. J Clin Pharm Ther 2018;43:606-13. |
| 68. | Cho HJ, Hong SJ, Park S. Knowledge and beliefs of primary care physicians, pharmacists, and parents on antibiotic use for the pediatric common cold. Soc Sci Med 2004;58:623-9. |
| 69. | Panagakou SG, Papaevangelou V, Chadjipanayis A, Syrogiannopoulos GA, Theodoridou M, Hadjichristodoulou CS. Risk factors of antibiotic misuse for upper respiratory tract infections in children: Results from a cross-sectional knowledge-attitude-practice study in Greece. ISRN Pediatr 2012;2012:685302. |
| 70. | Rousounidis A, Papaevangelou V, Hadjipanayis A, Panagakou S, Theodoridou M, Syrogiannopoulos G, et al. Descriptive study on parents' knowledge, attitudes and practices on antibiotic use and misuse in children with upper respiratory tract infections in Cyprus. Int J Environ Res Public Health 2011;8:3246-62. |
| 71. | Yuling P, de la Puente M. Census Bureau Guideline for the Translation of Data Collection Instruments and Supporting Materials: Documentation on how the Guideline was Developed. U.S. Census Bureau; 2005. Available from: https://www.census.gov/srd/papers/pdf/rsm2005-06.pdf. [Last accessed on 2019 Mar 30]. |
| 72. | Kamata K, Tokuda Y, Gu Y, Ohmagari N, Yanagihara K. Public knowledge and perception about antimicrobials and antimicrobial resistance in Japan: A national questionnaire survey in 2017. PLoS One 2018;13:e0207017. |
| 73. | Fernandes R, Naik S, Bhat AG, Shetty R, Hande MH, Ghafur A, et al. Knowledge assessment of E-bug assisted antimicrobial resistance education module in class VII school students of South Indian coastal town of Manipal. J Clin Med 2019;8. pii: E84. |
| 74. | King S, Exley J, Taylor J, Kruithof K, Larkin J, Pardal M. Antimicrobial stewardship: The effectiveness of educational interventions to change risk-related behaviours in the general population: A systematic review. Rand Health Q 2016;5:2. |
| 75. | Price L, Gozdzielewska L, Young M, Smith F, MacDonald J, McParland J, et al. Effectiveness of interventions to improve the public's antimicrobial resistance awareness and behaviours associated with prudent use of antimicrobials: A systematic review. J Antimicrob Chemother 2018;73:1464-78. |
| 76. | Sharma C, Rokana N, Chandra M, Singh BP, Gulhane RD, Gill JP, et al. Antimicrobial resistance: Its surveillance, impact, and alternative management strategies in dairy animals. Front Vet Sci 2017;4:237. |
| 77. | Ayukekbong JA, Ntemgwa M, Atabe AN. The threat of antimicrobial resistance in developing countries: Causes and control strategies. Antimicrob Resist Infect Control 2017;6:47. |
| 78. | Sakeena MH, Bennett AA, McLachlan AJ. Non-prescription sales of antimicrobial agents at community pharmacies in developing countries: A systematic review. Int J Antimicrob Agents 2018;52:771-82. |
| 79. | Dixon J, Duncan CJ. Importance of antimicrobial stewardship to the English National Health Service. Infect Drug Resist 2014;7:145-52. |
[Figure 1]
[Table 1], [Table 2]
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