Abstract
Objectives:
The present study was carried out to identify and report the pattern of antibiotics prescribing to determine the adherence to the international empirical and therapeutic guidelines of antibiotic use.
Methods:
A point prevalence survey took place at a selected date of January 26, 2020, in which data collection was performed to all the patients present in the hospital who used at least one systemic antibiotic agent as an inpatient from 00:00 am until midnight of that day. This was performed using European Surveillance of Antimicrobial Consumption (ESAC – audit tool). The participated hospital in this point prevalence study represents a major government hospital in the UAE. Descriptive statistics were used and results were expressed using standard statistical methods.
Results:
Out of the 125 hospitalized patients, a total of 41 (32.8%) patients were included in the survey and treated with different trends of antibiotics on the date point prevalence survey. The total number prescribed antibiotics was 54 with a higher percentage of treatment indication (70.4%), compared to prophylaxis indication (29.6%). The combinations of penicillin’s win in being the most commonly used agents by a percent of 31.5%, including the use of Amoxicillin-clavulanic acid by 22.2% and Piperacillin-tazobactam with 9.3%. The compliance with local/international guidelines accounts for 78.0% of the treated & prophylaxis patients.
Conclusions:
Considerable results have been obtained which can assure the quality improvement of the antibiotic use in the studied hospital.
Keywords: prevalence survey, antibiotic, prescribing, hospital, secondary care, UAE
INTRODUCTION
Throughout the history of medicine, antibiotics have been one of the most powerful fighters in a war against deadly organisms.1 Imprudent antibiotic use is a well-established risk factor which has been shown, worldwide, to be associated with the acquisition of infections involving Clostridium difficile (CD), methicillin resistant Staphylococcus aureus (MRSA) and extended-spectrum beta-lactamase (ESBL)-producing organisms.2-6 Clostridium difficile, a spore-forming gram-positive anaerobic bacillus, is a common pathogen in healthcare settings. The clinical spectrum of Clostridium difficile infection (CDI) ranges from uncomplicated diarrhea to severe life-threatening pseudomembranous colitis.7,8 Several studies have identified a growing resistance pattern to antibiotics due to the increased use of existing antibiotics9,10 and the slow pace of new antibiotic discovery.11 This has resulted in an international public health crisis of antimicrobial resistance,10,12 which represents a great threat to the humankind.13,14 In some countries, including the European Union, the disseminated risk of antibiotic resistance introduced devastating tragedy and has reached alarming levels 15,16 with a paradigm shift in prescribing patterns to broader spectrum agents of antibiotics in the last several decades.9 In the Middle East region, such as Saudi Arabia and Egypt, high prescribing rates of broad-spectrum antibiotics were identified in one study, which identified high resistance rates to antibiotics in the hospital settings.9 The continued emergence of both CDI and pathogens that produce beta-lactamase enzymes pose significant therapeutic implications, i.e. complicated therapy and limited treatment options, predisposing infected patients to higher mortality rates, longer hospital stays, higher antibiotic usage, increased treatment expenditure and causing considerable challenges for infection control.5,7 In one study conducted in 2003, it was shown that in the United States (US) alone, over than 7 billion dollars were consumed to treat both community and hospital-acquired infections (HAIs) associated with different bacterial strains. However, for the treatment of the hospital-acquired infections alone, around 4 billion dollars were consumed in the US due to the developed bacterial resistance to the over-prescribed antibiotics.9 The effective use of antibiotics with the appropriate practices and guidelines is of considerable importance to reduce and/or prevent the associated developed antibiotic resistance. On the other hand, the ineffective use of the antibiotics has been primarily associated with the disseminated resistance of different bacterial strains, including hospital-acquired infections.1,16 Despite the importance of education and guideline-based strategies within antibiotic stewardship programmes, it is frequently reported that compliance with such guidelines is relatively low.17 This point prevalence study aims to identify and report the pattern of antibiotics prescribing in one of the major hospitals in the UAE, to determine the adherence to the international empirical and therapeutic guidelines of antibiotic use, e.g. Infectious Diseases Society of America (IDSA) and National Institute for Heath and Care Excellence (NICE).
METHODS
Study setting
The participated hospital in this point prevalence study represents a major government hospital in the UAE at the time the research was conducted. The Hospital provides health care services in variety of specialty including general surgery, pediatrics, critical care, urology, orthopedics, ophthalmology, Ear-Nose-Throat (ENT) surgery, neurosurgery, vascular surgery, thoracic surgery, maxillofacial surgery, plastic surgery, accident & emergency and out-patient services. A total of 6 wards of the hospital were included in the survey to examine the risk of HAI. This includes the intensive care unit (ICU), surgical, pediatric and other wards. Under the umbrella of infection prevention and control committee, antibiotic Stewardship programme launched in Saqr hospital in January of 2014. In October, 2017, a nominated hospital Antibiotic Stewardship Committee was formulated, which represented multidisciplinary team, including physician leader and clinical pharmacist as coordinator of the committee. Additional team member included surgeon, anesthetist, pediatrician, internal medicine specialist, clinical microbiologist, infection control practitioner, nurse and quality staff. During the study period, the hospital bed capacity was 125 beds. During the month of January, the highest bed occupancy date was 26 January 2020.
Compliance with ethical standards
All procedures performed in this study involving human participants were in accordance with the ethical standards of the institutional and/or national research committees and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. For the purposes of conducting this study, governance approvals were obtained from the Ministry of Health and Prevention Research Ethics Committee RAK Subcommittee (Reference No: MOHAP/REC/2019/36 -2020-F- P). For this type of study (retrospective in design), formal individual patient consent was not required by the MOHAP Research Ethics Committee.
Study design
The survey took place at a selected date of January 26, 2020, in which data collection was performed to all the patients present in the hospital who used at least one systemic antibiotic agent as an inpatient from 00:00 am until midnight of that day to investigate the pattern of antibiotics prescribing. Any patient on only anti-retroviral, anti-tuberculosis, and anti-parasitic, antifungal, or antiviral agent medications or present in emergency room who were not yet admitted or patients who were treated as an out-patient were all excluded from the survey. Each detail about the prophylaxis and the given therapy was collected, considering also the prophylactic antibacterial if it were given for the surgical patients during the last 24 hours.
Antibiotic guidelines
The determination of the patient plan of therapy was assessed (either compliant or non-compliant) based on hospital antibiotic surgical prophylaxis guideline, and international guidelines from IDSA such as urinary tract infection, respiratory tract infection and skin & soft tissue infection.
Outcome measures
The antibiotic prescription prevalence was basically determined on the day of the survey by taking a percentage of the number of the patients getting antibiotic out of the whole number of patients exist as inpatients in the studied hospital.
Data collection
Data was extracted from the system with no direct contact with the patients. However, the hospital staff of clinical pharmacists was responsible to review patients’ notes of the antibiotic prescribing patterns. This was performed using European Surveillance of Antimicrobial Consumption (ESAC – tool). The collected data included details on patients’ demographics such as age, gender and other details of the prescribed antibiotics (e.g., strength, generic name, route of administration, dose and frequency). The number of inpatients included in each ward, admission source (home, other hospital, other department), duration of the hospital stays and the anatomical site of each treated infection were collected. Data regarding the local and/or international guidelines compliance of the hospital was documented based on the treatment indication; HAIs, community-acquired infection, surgical prophylaxis or medical.
Definitions
Community-acquire infections’ definition was explained as cases in which the antibiotic use or symptoms appear in less than two days (48 hours) after hospital admission. In contrast, when symptoms start at 48 hours or more of an admission to hospital, it is defined as a hospital-acquired infections (HAI) case. Compliance with the local /international guidelines for prescribing antibiotics was assessed through a “yes” or “no” question in the survey.
Statistical analysis
Descriptive statistics were used and results were expressed using standard statistical methods such as median, interquartile range and frequency (%). The statistical analyses were performed on SPSS for Windows (Advanced Statistics Release 25.0, SPSS® Inc, Chicago).
RESULTS
Data from the studied hospital was obtained with variations in several variables. The general characteristics of the point prevalence study population are shown in Table 1. Out of the 125 hospitalized patients, a total of 41 (32.8%) patients were included in the survey, and treated with different trends of antibiotics on the date of point prevalence survey, as shown in Table 1. The majority of treated patients were male 31 (75.6%), while the female patients were 10 (24.4%), with a median duration of hospitalization of 5 days. Of the 41 treated patients, the median age was 31 years. The total number prescribed antibiotics was 54 with a higher percentage of treatment indication (n= 38, 70.4%), compared to prophylaxis indication (n= 16, 29.6%). The greater usage of parental antibiotics was observed (n= 42, 77.8%), in contrast to oral antibiotics (n= 12, 22.2%). Different indications of the prescribed antibiotics were observed; HAI had the lowest indication (n= 3, 7.3%), compared to community-acquired infection indication (n= 24, 58.5%), surgical prophylaxis (n= 7, 17.1%) and others (n= 7, 17.1%). The most common anatomical site of the infection was the respiratory system (34.1%), compared to the skin and soft tissues (39.0%), the urinary system (9.8%), the gastrointestinal system (7.3%), Otolargycology (2.4%) and the cardiovascular system (2.4%). Out of the 41 treated patients included in the study, more than half were admitted to the surgical ward (51.2%), 19.5% were admitted to the pediatric ward, 4.9% were admitted to the intensive care unit (ICU) and 24.4% were admitted to the other wards in the hospital. In the studied hospital, the compliance with local/international guidelines accounts for 78.0% of the treated & prophylaxis patients.
Table 1.
General Characteristics of the study population, in participating study hospital, the point prevalence survey in Jan 2020, sample size=125
| Characteristics | Participating study hospital, Jan 2020 |
|---|---|
| Number of hospitalized patients | 125 |
| Number of treated patients, n (%) | 41 (32.8%) |
| Number of prescribed antibiotics | 54 |
| Age of treated patients, median (Interquartile range), years | 31.0 (11.0-43.0) |
| Duration of hospital stay, median (Interquartile range), days | 5 (2.0-9.0) |
| Gender, n (%) | |
| • Male | 31 (75.6) |
| • Female | 10 (24.4) |
| Admission source | |
| • Home | 35 (85.4) |
| • Other hospital | 6 (14.6) |
| • Another department | 0 (0.0) |
| Admission ward, n (%) | |
| • Intensive care unit | 2 (4.9) |
| • Surgical | 21 (51.2) |
| • Pediatric | 8 (19.5) |
| • Others | 10 (24.4) |
| Specialty, n (%) | |
| • Medical | 8 (19.5) |
| • Surgical | 33 (80.5) |
| • Intensive care unit | 0 (0.0) |
| • Others | 0 (0.0) |
| Antibiotic rout of administration, n (%) | |
| • Oral | 12 (22.2) |
| • Intravenous | 42 (77.8) |
| Antibiotic indication, n (%) | |
| • Treatment | 38 (70.4) |
| • Prophylaxis | 16 (29.6) |
| Anatomical site, n (%) | |
| • Respiratory system | 14 (34.1) |
| • Cardiovascular system | 1 (2.4) |
| • Gastrointestinal system | 3 (7.3) |
| • Urinary system | 4 (9.8) |
| • Skin, soft tissues | 16 (39.0) |
| • Otolargycology | 3 (7.3) |
| Duration of surgical prophylaxis, n (%) | |
| • Single dose | 0 (0.0) |
| • One day | 6 (37.5) |
| • More than One day, n (%) | 10 (62.5) |
| Compliance with local/international guidelines | |
| • No | 9 (22.0) |
| • Yes | 32 (78.0) |
| Indication of antibiotic treatment (diagnosis), n (%) | |
| • Hospital- acquired infection (HAI) | 3 (7.3) |
| • Community-acquired infection (CAI) | 24 (58.5) |
| • Surgical prophylaxis | 7 (17.1) |
| • Others | 7 (17.1) |
Getting to the results of Table 2, which represents the antibiotic agents prescribed in the participating hospital. The combinations of penicillin’s win in being the most commonly used agents by a percent of 31.5%, including the use of Amoxicillin-clavulanic acid by 22.2% and Piperacillin-tazobactam with a 9.3%. Then it’s followed by the third-generation cephalosporin’s, which takes a percent of 18.6%. The second most prescribed antibiotics were including Ceftazidime with a 13% and Cefotaxime with a 5.6%. The other most commonly used antibiotic was the following: second-generation cephalosporin’s (14.8%), which includes Cefuroxime (11.1%) and Cefprozil (3.7%), in addition to macrolides with a 7.4 % for Azithromycin and Clarithromycin (both with a 3.7% of use). Carbapenems (5.6%) for the use of Meropenem. Fluoroquinolones (7.4%) for the use of ciprofloxacin. Finally, Tetracyclines (1.9%) goes for the use of Tigecycline.
Table 2.
Antibiotic agents prescribed, with participating hospital, during the point-prevalence survey Jan 2020, sample size=125
| Antibiotic prescriptions | Number (%) |
|---|---|
| Tetracyclines (J01AA) | 1 (1.9) |
| • Doxycycline | 0 (0.0) |
| • Tigecycline | 1 (1.9) |
| Penicillins with extended spectrum (J01CA)) | 0 (0.0) |
| • Amoxicillin | 0 (0.0) |
| Beta-lactamase-sensitive penicillins (J01CE) | 0 (0.0) |
| • Phenoxymethylpenicillin | 0 (0.0) |
| • Benzylpenicillin | 0 (0.0) |
| Beta-lactamase-resistant penicillins (J01CF) | 0 (0.0) |
| Combinations of penicillins (J01CR) | 17 (31.5) |
| • Amoxicillin-clavulanic acid | 12 (22.2) |
| • Piperacillin-tazobactam | 5 (9.3) |
| First-generation cephalosporins (J01DB) | 0 (0.0) |
| • Cefalexin | 0 (0.0) |
| Second-generation cephalosporins (J01DC) | 8 (14.8) |
| • Cefuroxime | 6 (11.1) |
| • Cefprozil | 2 (3.7) |
| Third-generation cephalosporins (J01DD) | 10 (18.6) |
| • Cefotaxime | 3 (5.6) |
| • Ceftazidime | 7 (13.0) |
| • Ceftriaxone | 0 (0.0) |
| Monobactams (J01DF) | 0 (0.0) |
| • Aztreonam | 0 (0.0) |
| Carbapenems (J01DH) | 3 (5.6) |
| • Meropenem | 3 (5.6) |
| Trimethoprim and derivatives (J01EA) | 0 (0.0) |
| • Combination of trimethoprim/ | 0 (0.0) |
| sulfamethoxazole (J01EE) | 0 (0.0) |
| Macrolides (J01FA) | 4 (7.4) |
| • Erythromycin | 0 (0.0) |
| • Azithromycin | 2 (3.7) |
| • Clarithromycin | 2 (3.7) |
| Lincosamides (J01FF) 6 (0.9) | 0 (0.0) |
| • Clindamycin | 0 (0.0) |
| Aminoglycosides (J01GB) | 0 (0.0) |
| • Gentamicin | 0 (0.0) |
| • Tobramycin | 0 (0.0) |
| Fluoroquinolones (J01MA) | 4 (7.4) |
| • Ofloxacin | 0 (0.0) |
| • Levofloxacin | 0 (0.0) |
| • Ciprofloxacin | 4 (7.4) |
| Glycopeptide antibacterials (J01XA) | 2 (3.7) |
| • Vancomycin | 2 (3.7) |
| • Teicoplanin | 0 (0.0) |
| Steroid antibacterials (J01XC) | 1 (1.9) |
| Imidazole derivatives (J01XD) | 4 (7.4) |
| Nitrofuran derivatives (J01XE) | 0 (0.0) |
| Other antibacterials (J01XX) | 0 (0.0) |
| • Linezolid | 0 (0.0) |
| Chloramphenicol (J01BA) | 0 (0.0) |
DISCUSSION
Resistance to antibiotics is an international public concern. However, it is a local concern at its first stage.17 The considerable misuse of the antibiotics is a major cause of the global antibiotic Resistance.18 Therefore, it is very crucial to search for the weakness points in using the antibiotics in hospitals, and therefore, work on areas of improvement.1 Accordingly, local evaluation of the followed patterns of antibiotic prescribing is fundamental for the antibiotic stewardship program.18 The aim of this point prevalence study is to assess the local antibiotic prescribing patterns in one of the major government hospitals in emirate of Ras Al Khaimah in the UAE, and to determine the compliance with the international and local guidelines for antibiotic prescribing. The overall adherence percentage to the established guidelines was 78.0%. In fact, it can be very helpful in the monitoring and identifying the effectiveness of the antimicrobial stewardship program by the process of having a repeated point – prevalence surveys at the same setting,19 in addition to the inexpensive nature of the method.1
The prevalence of the antibiotic usage in the studied hospital was 32.8%. Interestingly, the highest prevalence was accounted for the antibiotics treating the community-acquired infections (58.5%), which in its turn reflect the high load within the healthcare system and its resources. The penicillins were shown to have the highest prescribing percentage following by the third generation cephalosporins. The prescribing patterns of fluoroquinolones, carbapenems and WHO AWaRe-reserve antibiotics in the study site were low. This represents a good compliance in the guidelines as this reduces c. difficile (CDI) as well as methicillin-resistant Staphylococcus aureus (MRSA) infections.3,4,20 Good clinical practices were observed with a high percentage representing good compliance with the international prescribing guidelines and may be related to early establishment of antibiotic stewardship programme.
Nonetheless, considerations must be given for the high prescribing patterns of the penicillin amoxicillin-clavulanic acid as it was manifested as one risk factor for acquiring CDI and MRSA.3,4,20 Therefore, future optimization for its prescribing is encouraged. The findings of this study are consistent with other reported studies in Northern Ireland, Turkey and China.1,21,22 In the previous study conducted in Northern Ireland which in a total of five hospital setting. In fact, slight differences in findings have been found possibly due to either the different patient cases itself, or some local difference in interpreting and using the guidelines.
The current study investigated the appropriate implementation of antibiotic stewardship program and its importance, it evaluated the guidelines implementation besides the physicians’ adherence to them. The study showed that cephalosporins and penicillins were the most commonly used agents as surgical prophylaxis. This comes in line with previous studies that showed a single dose of cefazolin antibiotic was the most frequently administered operative antibiotic prophylaxis.23,24 Additionally, these latter findings agree with the recommendation of NICE clinical guidelines (2011) regarding the best antibiotic selection and time to administer antibiotic prophylaxis.23,24 The study findings encourage the importance of the clinical pharmacist in making the physicians have a better compliance to the guidelines, which shows the benefit of involving the clinical pharmacist during the stewardship program.
In summary, this study has implemented very important points regarding the hospital antibiotic guidelines. Starting from the importance and the benefits of using European Surveillance of Antimicrobial Consumption (ESAC – audit tool) which is a simplified audit tool that helped in showing a quit important detail about the prescribing patterns of antibiotics in hospitals. Overall, the point prevalence survey must be taken in consideration as it showed to be very effective in improving the antibiotic therapy, mostly in secondary healthcare settings as they provide a very valuable information that indeed help in optimizing the antibiotic use, targeting quality improvement and reducing the resistance surveillance.
Study strengths and limitations
The study has flowing limitation: the retrospective nature of the study makes it susceptible to the effects of biases and confounding.
CONCLUSION
Considerable results have been obtained which can assure the quality improvement of the antibiotic use. Furthermore, the study has shown a better adherence to the hospital / international guidelines regarding the antibiotic use with an overall rate of 78%. With low prevalence of the antibiotic usage 32.8 %.
DECLARATIONS OF INTEREST
None.
FINANCIAL SUPPORT
This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.
DATA AVAILABILITY
The datasets generated during the current study are available from the corresponding author on reasonable request.
PATIENT CONSENT FOR PUBLICATION
Not required.
AUTHORSHIP STATEMENT
All authors have contributed significantly to the publication. Their contributions meet the criteria for authorship. All authors reviewed and approved the final draft of the submitted manuscript.
CONFLICTS OF INTEREST STATEMENT
No declarations of interest to be mentioned. This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.
ETHICS STATEMENT
For the purposes of conducting this study, governance approvals were obtained from the Ministry of Health and Prevention Research Ethics Committee RAK Subcommittee (Reference No: MOHAP/REC/2019/36 -2020-F- P).
Contributor Information
Munther S. Alnajjar, Department of Biopharmaceutics & Clinical Pharmacy, Faculty of Pharmacy, Al-Ahliyya Amman University, Amman, Jordan. malnajjar01@qub.ac.uk
Duaa Salem Jawhar, Pharmacy Department, Saqr Hospital, Emirates Health Services Establishment, Ras Al Khaimah, United Arab Emirates. duaa.jawhar@ehs.gov.ae.
Salah Aburuz, College of Medicine and Health Sciences, The United Arab Emirates University, Al Ain, United Arab Emirates. Faculty of Pharmacy, The University of Jordan, Amman. Jordan. saburuz@uaeu.ac.ae.
Dima A. Saeed, School of Pharmacy, Middle East University, Amman, Jordan. dsaeed01@qub.ac.uk
Ameerah Hasan Ibrahim, Department of Pharmacy, Faculty of Pharmacy, Al-Zaytoonah University of Jordan, Amman, Jordan. ameerah.ibrahim@zuj.edu.jo.
References
- 1.1. Alahmadi Y, Aldeyab M, Scott M. Point-prevalence surveys of antibiotic use and HAIs. Hospital Pharmacy Europe Pharmacy practice). 2016;84:27-29.; Alahmadi Y, Aldeyab M, Scott M. Point-prevalence surveys of antibiotic use and HAIs. Hospital Pharmacy Europe Pharmacy practice) 2016;84:27–29. [Google Scholar]
- 2.2. Vernaz NC, Huttner B, Muscionico D. Modelling the impact of antibiotic use on antibiotic-resistant Escherichia coli using population-bases data from a large hospital and its surrounding community. J Antimicrob Chemother. 2011;66(4):928-935. https://doi.org/10.1093/jac/dkq525 [DOI] [PubMed]; Vernaz NC, Huttner B, Muscionico D. Modelling the impact of antibiotic use on antibiotic-resistant Escherichia coli using population-bases data from a large hospital and its surrounding community. J Antimicrob Chemother. 2011;66(4):928–935. doi: 10.1093/jac/dkq525. [DOI] [PubMed] [Google Scholar]
- 3.3. Hao H, Dai M, Wang Y, et al. Key genetic elements and regulation systems in methicillin-resistant Staphylococcus aureus. Future Microbiol. 2012;7(11):1315-1329. https://doi.org/10.2217/fmb.12.107 [DOI] [PubMed]; Hao H, Dai M, Wang Y, et al. Key genetic elements and regulation systems in methicillin-resistant Staphylococcus aureus. Future Microbiol. 2012;7(11):1315–1329. doi: 10.2217/fmb.12.107. [DOI] [PubMed] [Google Scholar]
- 4.4. Aldeyab MA, Scott MG, Kearney M. Impact of an enhanced antibiotic stewardship on reducing methicillin-resistant Staphylococcus aureus in primary and secondary healthcare settings. Epidemiol Infect. 2014;142(3):494-497. https://doi.org/10.1017/S0950268813001374 [DOI] [PMC free article] [PubMed]; Aldeyab MA, Scott MG, Kearney M. Impact of an enhanced antibiotic stewardship on reducing methicillin-resistant Staphylococcus aureus in primary and secondary healthcare settings. Epidemiol Infect. 2014;142(3):494–497. doi: 10.1017/S0950268813001374. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 5.5. Self WH, Wunderink RG, Williams DJ. Staphylococcus aureus Community-acquired Pneumonia:Prevalence, Clinical Characteristics, and Outcomes. Clin Infect Dis. 2016;63(3):300-310. [DOI] [PMC free article] [PubMed]; Self WH, Wunderink RG, Williams DJ. Staphylococcus aureus Community-acquired Pneumonia:Prevalence, Clinical Characteristics, and Outcomes. Clin Infect Dis. 2016;63(3):300–310. doi: 10.1093/cid/ciw300. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 6.6. Ledda A, Price JR, Cole K. Re-emergence of methicillin susceptibility in a resistant lineage of Staphylococcus aureus. J Antimicrob Chemother. 2017;72(5):1285-1284. https://doi.org/10.1093/jac/dkw570 [DOI] [PMC free article] [PubMed]; Ledda A, Price JR, Cole K. Re-emergence of methicillin susceptibility in a resistant lineage of Staphylococcus aureus. J Antimicrob Chemother. 2017;72(5):1285–1284. doi: 10.1093/jac/dkw570. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 7.7. Thompson I. Clostridium difficile-associated disease:update and focus on non-antibiotic strategies. Age Ageing. 2008;37(1):14-8. https://doi.org/10.1093/ageing/afm159 [DOI] [PubMed]; Thompson I. Clostridium difficile-associated disease:update and focus on non-antibiotic strategies. Age Ageing. 2008;37(1):14–8. doi: 10.1093/ageing/afm159. [DOI] [PubMed] [Google Scholar]
- 8.8. Planche T. Clostridium difficile. Prevention and Control of Infection. 2013;41:654-655.; Planche T. Clostridium difficile. Prevention and Control of Infection. 2013;41:654–655. [Google Scholar]
- 9.9. Al Matar M, Enani M, Binsaleh G. Point prevalence survey of antibiotic use in 26 Saudi hospitals in 2016. J Infect Public Health. 2019;12(1):77-82. https://doi.org/10.1016/j.jiph.2018.09.003 [DOI] [PubMed]; Al Matar M, Enani M, Binsaleh G. Point prevalence survey of antibiotic use in 26 Saudi hospitals in 2016. J Infect Public Health. 2019;12(1):77–82. doi: 10.1016/j.jiph.2018.09.003. [DOI] [PubMed] [Google Scholar]
- 10.10. Pakyz AL, MacDougall C, Oinonen M. Trends in antibacterial use in US academic health centers:2002 to 2006. Arch Intern Med. 2008;168(20):2254-2260. https://doi.org/10.1001/archinte.168.20.2254 [DOI] [PubMed]; Pakyz AL, MacDougall C, Oinonen M. Trends in antibacterial use in US academic health centers:2002 to 2006. Arch Intern Med. 2008;168(20):2254–2260. doi: 10.1001/archinte.168.20.2254. [DOI] [PubMed] [Google Scholar]
- 11.11. Hulscher ME, van der Meer JW, Grol RP. Antibiotic use:how to improve it?Int J Med Microbiol. 2010;300(6):351-356. https://doi.org/10.1016/j.ijmm.2010.04.003 [DOI] [PubMed]; Hulscher ME, van der Meer JW, Grol RP. Antibiotic use:how to improve it? Int J Med Microbiol. 2010;300(6):351–356. doi: 10.1016/j.ijmm.2010.04.003. [DOI] [PubMed] [Google Scholar]
- 12.12. Almomani BA, Khasawneh RA, Saqan R. Predictive utility of prior positive urine culture of extended- spectrum β-lactamase producing strains. PLoS One. 2020;15(12):e0243741. https://doi.org/10.1371/journal.pone.0243741 [DOI] [PMC free article] [PubMed]; Almomani BA, Khasawneh RA, Saqan R. Predictive utility of prior positive urine culture of extended- spectrum β-lactamase producing strains. PLoS One. 2020;15(12):e0243741. doi: 10.1371/journal.pone.0243741. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 13.13. Robert J, Péan Y, Varon E, et al. Surveillance de la prescription des antibiotiques (SPA) Group. Point prevalence survey of antibiotic use in French hospitals in 2009. J Antimicrob Chemother. 2012;67(4):1020-1026. 10.1093/jac/dkr571 [DOI] [PubMed]; Robert J, Péan Y, Varon E, et al. Surveillance de la prescription des antibiotiques (SPA) Group. Point prevalence survey of antibiotic use in French hospitals in 2009. J Antimicrob Chemother. 2012;67(4):1020–1026. doi: 10.1093/jac/dkr571. 10.1093/jac/dkr571. [DOI] [PubMed] [Google Scholar]
- 14.14. Infectious Diseases Society of America (IDSA), Spellberg B, Blaser M, Guidos RJ. Combating antimicrobial resistance:policy recommendations to save lives. Clin Infect Dis. 2011;52(Suppl 5):S397-428. https://doi.org/10.1093/cid/cir153 [DOI] [PMC free article] [PubMed]; Infectious Diseases Society of America (IDSA) Spellberg B, Blaser M, Guidos RJ. Combating antimicrobial resistance:policy recommendations to save lives. Clin Infect Dis. 2011;52(Suppl 5):S397–428. doi: 10.1093/cid/cir153. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 15.15. Stichele RHV, Elseviers MM, Ferech M. European surveillance of antimicrobial consumption (ESAC):data collection performance and methodological approach. Br J Clin Pharmacol. 2004;58(4):419-428. https://doi.org/10.1111/j.1365-2125.2004.02164.x [DOI] [PMC free article] [PubMed]; Stichele RHV, Elseviers MM, Ferech M. European surveillance of antimicrobial consumption (ESAC):data collection performance and methodological approach. Br J Clin Pharmacol. 2004;58(4):419–428. doi: 10.1111/j.1365-2125.2004.02164.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 16.16. Dumpis U, Balode A, Vigante D. Prevalence of nosocomial infections in two Latvian hospitals. Euro Surveill. 2003;8(3):73-78. https://doi.org/10.2807/esm.08.03.00405-en [DOI] [PubMed]; Dumpis U, Balode A, Vigante D. Prevalence of nosocomial infections in two Latvian hospitals. Euro Surveill. 2003;8(3):73–78. doi: 10.2807/esm.08.03.00405-en. [DOI] [PubMed] [Google Scholar]
- 17.17. MacDougall C, Polk RE. Antimicrobial stewardship programs in health care systems. Clin Microbiol Rev. 2005;18(4):638-656. https://doi.org/10.1128/CMR.18.4.638-656.2005 [DOI] [PMC free article] [PubMed]; MacDougall C, Polk RE. Antimicrobial stewardship programs in health care systems. Clin Microbiol Rev. 2005;18(4):638–656. doi: 10.1128/CMR.18.4.638-656.2005. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 18.18. Aldeyab MA, Kearney MP, McElnay JC, et al. A point prevalence survey of antibiotic use in four acute-care teaching hospitals utilizing the European Surveillance of Antimicrobial Consumption (ESAC) audit tool. Epidemiol Infect. 2012;140(9):1714-1720. https://doi.org/10.1017/S095026881100241X [DOI] [PubMed]; Aldeyab MA, Kearney MP, McElnay JC, et al. A point prevalence survey of antibiotic use in four acute-care teaching hospitals utilizing the European Surveillance of Antimicrobial Consumption (ESAC) audit tool. Epidemiol Infect. 2012;140(9):1714–1720. doi: 10.1017/S095026881100241X. [DOI] [PubMed] [Google Scholar]
- 19.19. Zarb P, Amadeo B, Muller A. Hospital Care Subproject Group. Identification of targets for quality improvement in antimicrobial prescribing:the web-based ESAC Point Prevalence Survey 2009. J Antimicrob Chemother. 2011;66(2):443-449. https://doi.org/10.1093/jac/dkq430 [DOI] [PubMed]; Zarb P, Amadeo B, Muller A. Hospital Care Subproject Group. Identification of targets for quality improvement in antimicrobial prescribing:the web-based ESAC Point Prevalence Survey 2009. J Antimicrob Chemother. 2011;66(2):443–449. doi: 10.1093/jac/dkq430. [DOI] [PubMed] [Google Scholar]
- 20.20. W H O. The 2019 WHO AWaRe classification of antibiotics for evaluation and monitoring of use. Geneva:World Health Organization;2019. https://apps.who.int/iris/handle/10665/327957; W H O. The 2019 WHO AWaRe classification of antibiotics for evaluation and monitoring of use. Geneva: World Health Organization; 2019. https: //apps.who.int/iris/handle/10665/327957 . [Google Scholar]
- 21.21. Usluer G, Ozgunes I, Leblebicioglu H. Turkish Antibiotic Utilization Study Group. A multicenter point-prevalence study:antimicrobial prescription frequencies in hospitalized patients in Turkey. Ann Clin Microbiol Antimicrob. 2005;4:16. https://doi.org/10.1186/1476-0711-4-16 [DOI] [PMC free article] [PubMed]; Usluer G, Ozgunes I, Leblebicioglu H Turkish Antibiotic Utilization Study Group. A multicenter point-prevalence study:antimicrobial prescription frequencies in hospitalized patients in Turkey. Ann Clin Microbiol Antimicrob. 2005;4:16. doi: 10.1186/1476-0711-4-16. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 22.22. Hu S, Liu X, Peng Y. Assessment of antibiotic prescription in hospitalised patients at a Chinese university hospital. J Infection. 2003;46(3):161-164. https://doi.org/10.1053/jinf.2002.1078 [DOI] [PubMed]; Hu S, Liu X, Peng Y. Assessment of antibiotic prescription in hospitalised patients at a Chinese university hospital. J Infection. 2003;46(3):161–164. doi: 10.1053/jinf.2002.1078. [DOI] [PubMed] [Google Scholar]
- 23.23. National Institute for Health and Clinical Excellence (NICE). Surgical site infection. NICE guideline. Draft for consultation. 2008. https://www.nice.org.uk/guidance; National Institute for Health and Clinical Excellence (NICE) Surgical site infection. NICE guideline. Draft for consultation. 2008. https: //www.nice.org.uk/guidance .
- 24.24. Alnajjar MS, Alashker DA. Surgical site infections following caesarean sections at Emirati teaching hospital:Incidence and implicated factors. Sci Rep. 2020;10(1):1⇾. https://doi.org/10.1038/s41598-020-75582-9 [DOI] [PMC free article] [PubMed]; Alnajjar MS, Alashker DA. Surgical site infections following caesarean sections at Emirati teaching hospital:Incidence and implicated factors. Sci Rep. 2020;10(1):18702. doi: 10.1038/s41598-020-75582-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Data Availability Statement
The datasets generated during the current study are available from the corresponding author on reasonable request.
