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 Table of Contents  
ORIGINAL ARTICLE
Year : 2019  |  Volume : 8  |  Issue : 1  |  Page : 47-53

Antibiotics' prescribing pattern in intensive care unit in Taif, Saudi Arabia


1 King Faisal Medical Complex, College of Pharmacy, Taif University, Taif, KSA
2 Deparment of Medical Biochemistry, Riyadh Elm University, Riyadh, KSA
3 Deparment of Pharmacology, College of Pharmacy, Taif University, Taif, KSA

Date of Web Publication16-May-2019

Correspondence Address:
Prof. Ahmed Salah Eldalo
Department of Pharmacology, College of Pharmacy, Taif University, Al-Haweiah, P.O. Box 888, Taif
KSA
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/sjhs.sjhs_12_19

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  Abstract 


Introduction: Antibiotics continue to be widely prescribed in critically ill patients, and they form a significant proportion of the total drugs consumed in the intensive care unit (ICU). Objective: The aim of the present study was to identify antibiotics prescribing patterns for patients admitted to ICU at King Faisal Medical Complex (KFMC), Taif, Saudi Arabia to assess the appropriate use of antibiotics and its compliance to the KFMC local guidelines. Materials and Methods: The study participants included all patients admitted for at least 48 h at the ICU in KFMC and received antibiotic(s). A prospective, observational study was carried out over a period of 3 months from August to October 2017. A standard clinical record form was used. Data were analyzed using Statistical Package for the Social Sciences (IBMSPSS, version 22). Results: From a total of 92 patients admitted to the ICU during the study, 429 antibiotic prescriptions were recorded that have been given to the patients, with an average of 4.6 antibiotics/prescription. Patients' average length of stay was 7.4 days. Ceftriaxone was the most frequently (21.7%) prescribed antibiotic followed by Tazocin® (17.7%), Metronidazole 15.1% and Meropenem 9.5%. Moreover, 69% of all prescribed antibiotics were compliant with the KFMC local guidelines. Conclusion: The high utilization rates of antibiotics prescribed during admission at KFMC's ICU were a matter of great concern. Therefore, they needed to be controlled by the use of local guidelines, surveillance, and antibiotic restriction policies of health care.

Keywords: Antibiotics, intensive care unit, prescribing pattern, Saudi Arabia


How to cite this article:
Alharthi NR, Kenawy G, Eldalo AS. Antibiotics' prescribing pattern in intensive care unit in Taif, Saudi Arabia. Saudi J Health Sci 2019;8:47-53

How to cite this URL:
Alharthi NR, Kenawy G, Eldalo AS. Antibiotics' prescribing pattern in intensive care unit in Taif, Saudi Arabia. Saudi J Health Sci [serial online] 2019 [cited 2019 Oct 22];8:47-53. Available from: http://www.saudijhealthsci.org/text.asp?2019/8/1/47/257762




  Introduction Top


Antimicrobials are important medicines and are commonly used in hospitals. The huge usage of antimicrobials leads to misuse and harmful impacts on the patients. The WHO defined the inappropriate usage of antimicrobial as; any prescribing antimicrobial agents without need or any improper dosage form, or short or long duration of treatment which usually leads to increase in the risk of resistance.[1]

The intensive care unit (ICU) is a hospital department for patients that suffer critical illnesses. The patients usually receive multiple medications from different pharmacological classes. The judicious use of these medications can be lifesaving. The use of conventional medicines may expose a substantial portion of ICUs' patients to drug-related problems such as drug-drug interactions, high risk of adverse effects, and treatment failure.[2] Furthermore, ICUs' patients are at risk of developing nosocomial infections. Antimicrobials are heavily prescribed in the (ICUs), especially those broad-spectrum ones. The bad practice enhances the antimicrobial resistance and increases the side effects of such drugs. On the other hand, it increases the unnecessary treatment costs on the patients.[3],[4]

Drug utilization study is a component of medical audit that aims to monitor and evaluate the drug prescription patterns and to suggest necessary modifications in the prescribing practices to achieve rational therapeutic practice as well as cost-effective health care. This is also applied on the high utilization rate of antibiotics in ICU which is a matter of great concern and needs to be evaluated. There is an urgent need to formulate rational antibiotic prescription policy and their strict implementation to prevent extensive use of antibiotics. Interventional programs should focus on infection control with rational antibiotic prescription aimed at minimizing unnecessary cost, adverse drug reaction, and emergence of bacterial resistance.[1]

Many studies have been conducted in different countries to evaluate the usage of antimicrobials in ICUs. A study in Northern India revealed that the antibiotics are one of the most prescribed medicines in the ICU especially for elderly and sever ill patients.[5] Another Indian study in tertiary care teaching hospital found that diverse drug classes were used in the ICU including antibiotics. The authors recommended the encouragement of rational use of antimicrobial agents in ICU by following strict hospital antimicrobial policy.[6] A multicenter cross-sectional observational study was carried out in ICUs of 8 countries in Latin America. It concluded that there is an urgent need of implementing an evidence-based stewardship program depending on the use of antimicrobials in the health-care setting.[7] A Qatari study emphasized the need for antibiotics prescribing guidelines and drug utilization review in the hospitals to minimize the emergence of multidrug resistance.[8] Al Ansari et al. admitted that the majority of patients in the ICU in Bahrain hospitals had antibiotics in their treatment course.[9]

The aim of this study was to identify antibiotics prescribing patterns for patients admitted to the ICU ward in King Faisal Medical Complex (KFMC) in Taif City, Saudi Arabia, to assess the appropriate use of antibiotics and its compliance to the KFMC local guidelines.


  Materials and Methods Top


Study design

A prospective observational study was carried out from August to November 2017.

Study setting

The study was conducted in the main ICUs in KFMC at Taif City, Saudi Arabia. KFMC is a referral center with a capacity of 300 beds covering all medical and surgical disciplines including the ICU for adults. The main ICU at KFMC consists of 25 beds in addition to two isolation rooms and managed by 2 consultants, 4 specialists, and 11 resident physicians.

Study population

All patients aged ≥12 years admitted to the ICU of KFMC for a minimum of 72 h and receiving a systemic antibiotic were included in the study. All patients admitted to emergency department (ED), transferred from KFMC (medical or surgical) departments, or transferred from other hospitals to ICU of KFMC during the study were included in the study.

Ethical considerations

This study approved by the Research Ethical Committee at Riyadh Colleges of Dentistry and Pharmacy through a research registration number FPGRP/43639013/148. Approval to perform the study in KFMC was obtained from the director of the hospital. Participants' information was kept confidential. All the policies and procedure of KFMC were followed and respected.

Study instrument

A standard clinical record form that was used included two main sections. Section one captured demographic data including patients' name, medical record number, age, weight, sex, diagnosis, and date of admission. Section two was about clinical indications for antimicrobial therapy, antimicrobial selection, dosing, route of administration, patients' creatinine clearance (for patients with chronic kidney disease or renal impairment patients), liver function test results, and compliance to local antibiotic therapy guidelines of each time points of the study.

Data were collected along with details of antibiotic therapy and infection-related investigations at 3 time points – day 0 (day of admission to ICU), day 3, and day 7 of admission or discharge day from ICU. Days calculated using the following equation: Total average length of stay (LOS) (in days) = (inpatient days of care/total admissions).

At day 0 of admission, all information for all patients were recorded based on the documentation available in the patients' chart and reports. First assessment of antibiotic prescriptions was done at this time point in which the antibiotic compliance to KFMC local guidelines or not was checked.

Second assessment of antibiotic prescriptions was done at day 3 of admission. All antibiotic prescriptions were reassessed for all recorded patients. The assessment was largely based on the culture sensitivity results at this point, and if de-escalation of antibiotic was done by treating physician or not.

Regarding the KFMC antibiotic policy, the treating physician should renew antibiotic orders every 7 days except for known cases that need long courses. Third or endpoint assessment was done at day 7 or patient discharge day (if the patient LOS was <7 days). All antibiotic prescriptions were reassessed again for all recorded patients to check if any change in treatment plan based on antibiotic orders updating, patient clinical situation, or culture sensitivity test results existed.

Rationality (compliance) according to King Faisal Medical Complex local guidelines

According to KFMC local guidelines, the therapy is considered rational if the antimicrobial use and its route of administration, dose, frequency, and duration of use were considered appropriate for infection. Therapy is considered irrational if the antimicrobial was used without indication, prophylaxis under circumstances of unproven efficacy, or by clearly inappropriate route, dose, or preparation for that indication. The therapy is considered questionable when insufficient clinical or laboratory data were present to enable the therapy to be classified as clearly rational or irrational. According to KFMC antibiotic policy and prescribing privileges; antibiotics are divided into three main groups: unrestricted agents that are prescribed by all physicians, restricted agents that are prescribed by specialist and consultants' physicians, and the last are reserved agents that are prescribed by consultants' physicians only.

Statistical analysis

The collected data were entered and analyzed using the Statistical Package of the Social Sciences (IBM SPSS, version 22, IBM Corp., Armonk, NY, USA). Means and frequencies were determined to obtain the percentage of all study variables.


  Results Top


A total of 92 patients were admitted to ICU matching inclusion criteria in this study with the majority being males 66 (71.7%). Most patients 46 (50%) were admitted directly to ICU from the ED whereas 42 (45.7%) of them were transferred from medical departments, as shown in [Table 1]. There were a variety of cases; respiratory tract infection was most common (29.35%), followed by central nervous system disorders (20.65%), then road traffic accidents (17.39%), as shown in [Figure 1]. The average LOS for 49 patients was from (2 to 5 days), for 27 patients was from (6 to 11 days), for 9 patients was from (11 to 15 days), and for 7 patients was more than 15 days [Table 1]. During the study, for all patients, the average LOS was 7.4. The patients' turnover was 4.6 days regarding ICU policy. [Table 1] shows that of 92 patients, 37 (40.2%) received one prescribed antibiotic, 36 (39.1%) patients had two antibiotics, and 17 (18.1%) had three prescribed antibiotics. At the 1st day of admission (day 0), a total of 166 antibiotic orders were prescribed as empiric therapy. Unfortunately, only 41 (24.7%) antibiotic susceptibility test (AST) were ordered before the initiation of antibiotics, while 125 (75.3%) antimicrobials were started without AST order. At second point assessment (day 3), a total of 169 antimicrobials were recorded, only new three prescriptions including antibiotics were added, two patients were existed, and the remaining were considered as continuation of a started empiric therapy. At the endpoint assessment (day 7) or during patients discharge from ICU, 94 antibiotics orders were recorded after discontinuation of antibiotics for some patients or during renewing antibiotic orders regarding KFMC antibiotic policy. Among all patients, 38 (41%) received antibiotics as prophylaxis while the remaining were given as treatment. [Figure 2] shows a total of 429 antibiotic' orders covering all patients at all study time points (day 0, day 3, and endpoint); 213 antibiotic orders were prescribed by resident physicians, 185 antibiotics' orders were prescribed by specialist physicians, and 31 antibiotics' orders were prescribed by consultant physicians. The most commonly prescribed antibiotics as empiric therapy ( first line) in the ICU were; ceftriaxone (21.91%), piperacillin + tazobactam (Tazocin®) (17.7%), and metronidazole (15.15%). Other prescribed antibiotics such as meropenem (9.56%), vancomycin, linezolid and moxifloxacin (5.59%), and amoxicillin/clavulanate (Augmentin®) (3.5%), as shown in [Table 2]. The compliance to KFMC local guidelines was recorded in each time point as presented in [Table 3]. At admission day (day 0), out of the 166 prescribed antibiotics, 110 (66%) were rational and compliant to KFMC local guidelines. At day 3, the assessment of which antibiotics had been deescalated. Of the 169 antibiotics, 117 (69%) prescribed antibiotics were compliant to KFMC local guidelines. At the end point, out of 94 prescribed antibiotics, 69 (73%) were compliant to KFMC local guidelines. The final compliance assessment to KFMC guidelines at all of study time points was that 296 (69%) antibiotic orders were compliant to KFMC local guidelines as shown in [Figure 3]. Among culture sensitivity reported in the study period, four dangerous multidrug-resistant pathogens were recorded; Pseudomonas aeruginosa multidrug resistant (MDR) was recorded 6 times, Acinetobacter baumannii MDR were recorded 3 times, methicillin-resistant Staphylococcus aureus (MRSA) were recorded 3 times, and extended-spectrum beta-lactamases (ESBL) were recorded only one time as shown in [Figure 4].
Table 1: General data about participants and antibiotic's used

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Figure 1: Percentage of admitting diseases for all patients in intensive care unit

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Figure 2: Distribution of antibiotic orders according to prescribing physicians in intensive care unit

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Table 2: Number and percentage of prescribing times for each antibiotics

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Table 3: Compliance of antibiotic orders to King Faisal Medical Complex local guidelines at each time point

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Figure 3: The final compliance assessment to King Faisal Medical Complex guidelines

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Figure 4: The presence of multidrug-resistant pathogen in King Faisal Medical Complex intensive care unit during study

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  Discussion Top


Patients admitted to ICU always suffer from critical illnesses and are usually exposed to hospital-acquired infections. These nosocomial infections are treated by heavy and poly antibiotics which may be accompanied by antimicrobial resistance, treatment failure, and increase the rate of mortality and morbidity.[10]

The current study was concerned with the use of antimicrobials in one of the most important ICUs in Taif City in the Western Region of Saudi Arabia. A total of 92 patients were investigated during this study, 29.35% of them complaining from disorders related respiratory system. This was in agreement with study results in India reported by Drupad et al.[6]

This study findings showed that the average LOS was 7.4 days which is higher than KFMC ICU policy which endorsed patients' turnover as 4.6 days. However, these results were in accordance with a study was done by Al Ansari et al., (2013) about drug patterns in ICU in the Kingdom of Bahrain that reported patients' average LOS was 7.5 days.[9] Regarding the antimicrobials' usage; the results of this study revealed that a total of 429 antibiotic prescriptions covered all study time points, the average number was 4.6 antibiotics per prescription. However, in an Indian study conducted by Williams et al., a mean of 5.1 drug per prescription were demonstrated.[5] Another study in Nepal reported a mean ± standard deviation number of antibiotics per prescription as 5.1 ± 2.7.[11] The average number of antibiotics per prescription is an important index of a prescription audit. It is recommended that the number of drugs per prescription should be kept as low as possible to minimize the risk of drug interactions, development of bacterial resistance, and hospital costs.[12] The results of the present investigations demonstrated that the most frequently prescribed antibiotics were ceftriaxone (21.9%), piperacillin/tazobactam (Tazocin®) (17.7%) followed by Metronidazole (15.1%) and Meropenem (9.5%). The reason for prescribing ceftriaxone and piperacillin/tazobactam as empirical therapy might be due to the fact that it covers majority of suspected microorganisms. The rationale behind prescribing metronidazole is that it covers the anaerobic infections. These results were in agreement with a study done by Drupad et al., about antimicrobial drug utilization in a medical ICU in a tertiary care teaching hospital in India. They reported that ceftriaxone, cefixime, and metronidazole were the most commonly prescribed antibiotics.[6] Colisin, meropenem, imipenem, tigecycline, and moxifloxacin are considered as restricted agents according to KFMC antibiotics prescribing policy which means that the prescription order should be made by consultant physicians only. However, the present work showed that these agents were prescribed 69 times by residents and specialist physicians which might indicate the ignorance of prescribing privileges policy. The present study showed that most antibiotics prescribed at day 0 were ordered as empiric treatment or prophylaxis or empiric therapy. They were based on initial diagnosis or clinical findings, and physicians experience regardless the local KFMC guidelines. KFMC guidelines reveal that the usage of antibiotics in ICU correlates with the infectious disease (ID) pattern, the causative microorganism, and patients' clinical outcomes. Moreover, results of this work demonstrated that the empirical therapy was continued in most cases, and the need for de-escalation of empirical therapy was less common. De-escalation of antibiotics means; changing broad-spectrum or multiple antimicrobials to narrow ones or target therapy, or discontinuing antimicrobials based on culture and susceptibility results.[13] Ohji et al., in a meta-analysis study in Japan reported that de-escalation therapy is a strategy used widely to treat infections while avoiding the use of broad-spectrum antimicrobials.[14] Unfortunately, the present study revealed that the term de-escalation was unknown among most ICU physician. Therefore, they were keeping continuation of empirical therapy, and their judgment was based on patients' clinical improvement. However, there is a paucity of clinical evidence to demonstrate the effectiveness and safety of de-escalation therapy compared to conventional therapy. In terms of first-choice antibiotics, the present work observed a widespread use of Tazocin®. This practice is justified by the high rates of P. aeruginosa in KFMC ICU. However, this practice is considered as a risk factor of developing Tazocin® resistant P. aeruginosa. This finding was in agreement with a study done by Harris et al., that reported an irrational use of Tazocin is considered as a strong risk factor for Tazocin®-resistant P. aeruginosa.[15] This study showed the presence of four dangerous MDR pathogen including P. aeruginosa MDR (6 times), A. baumannii MDR (3 times), MRSA 3 times, and ESBL one time. Reporting such MDR pathogens might reflect the irrational use of antibiotics in terms of selection, dosing adjustment, and duration of antibiotics regimen in the ICU of KFMC. In a study done by Ventola, authors reported that Acinetobacter MDR caused pneumonia or bloodstream infections, especially in critically ill patients on mechanical ventilation. Some Acinetobacter species have become resistant to all or nearly all antibiotics.[16] About 12,000 health care-acquired Acinetobacter infections occur in the U.S. each year; 7,300 (63%) of these are MDR to at least three different classes of antibiotics causing 500 deaths per year. Furthermore, P. aeruginosa was a common cause of hospital-acquired infections, including pneumonia and bloodstream, urinary tract, and surgical-site infections. More than 6000 (13%) out of the 51,000 health care-associated P. aeruginosa infections that occur in the U.S. each year were MDR. Roughly, 400 deaths per year were attributed to these infections. Some strains of MDR P. aeruginosa have been found to be resistant to nearly all antibiotics, including aminoglycosides, cephalosporins, fluoroquinolones, and carbapenems.[16] The findings of the present work reported that antibiotics were given as prophylaxis in 41% of the included patients. The results in this study revealed that the physicians prescribing the antibiotics based on their experiences, without taking into account the local guidelines or the clinical investigations. Schmitt et al., (2014) indicated that with regard to antibiotic prophylaxis, a clear distinction should be made between surgical and nonsurgical patients.[17] Many guidelines are available for surgical patients, and there is an agreement in recommending cefazolin, cefoxitin, and cefuroxime as the first choice, or ceftriaxone, ceftizoxime, and glycopeptides as the second choice, for no more than 24 h.

In regard to Saudi Ministry of Health, prescribing privilege policy should be followed strictly. ICU physicians in KFMC showed ignorance of these points of policy. The present results showed that the most frequently prescribed antibiotics were ordered by resident physicians without referring to consultants. This might be due to the work overload, consultant physicians' shortage, and absence of ID physicians. Lacking of ID physician was considered as a gap between all physicians' specialty in which more than one physician can share antibiotics prescribing. Unadjusted Medicare data suggest that ID specialists routinely care for a very complex patient population. Notably, on an unadjusted basis, ID intervention was associated with lower index stay mortality. After risk adjustment, ID care of patients with ID diagnoses was associated with better outcomes and lower cost of care.[12] The results of the current study revealed that only 41 antibiotic susceptibility tests (AST) were done before initiation of antibiotic therapy at the 1st day of admission to the ICU, while 125 antibiotics were started without AST orders. There were many reasons behind lacking of AST. For instance, some patients received antibiotic therapy as prophylaxis, where AST is not necessary, and microbiology laboratory capabilities might not be able to do all tests. In some circumstances, the reasons behind lacking of AST might be due to the ignorance of AST by treating physicians. In most situations, initial antimicrobial therapy is decided based on the clinical features of the patient. Situations become worse when antibiotic use started at the beginning of treatment then repeated microbiological cultures fail to confirm the pathogenic cause during the microbiological investigation.[4]

The implementation of evidence-based guidelines for the use of antimicrobials has been shown to improve the overall patients' outcomes. The presence of such guidelines is to help physicians to prescribe all appropriate antibiotics, avoid unjustified prescriptions, reduce the emergence of antibiotic-resistant bacteria, support high-quality clinical practice, and minimize unnecessary expenses. The present results revealed that 69% of all prescribed antibiotics were in compliance with KFMC local guidelines. A study by Badar and Navale about antimicrobial agents in medicine ICU in India reported that less than one-third of antimicrobials were rationally prescribed.[18] The main cause of noncompliance of antibiotics in the ICUs was the use of such medicines prior the admission to ICU.[19]


  Conclusion Top


The present study reveals that antibiotics continue to be widely prescribed to critically ill patients in KFMC and form a significant proportion of the total drugs consumed in the ICU. The high utilization rates of antibiotics prescribed at admission to KFMC's ICU are a matter of great concern and need to be urgently addressed by the use of guidelines, protocols, educational initiatives, and surveillance. Rational use of antimicrobial agents in ICU should be encouraged by following strict hospital antibiotic guidelines and policy.

Acknowledgment

The authors would like to thank all family members who accepted to participate in this study.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
  References Top

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Lockhart SR, Abramson MA, Beekmann SE, Gallagher G, Riedel S, Diekema DJ, et al. Antimicrobial resistance among gram-negative bacilli causing infections in intensive care unit patients in the United States between 1993 and 2004. J Clin Microbiol 2007;45:3352-9.  Back to cited text no. 2
    
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Esposito S, Leone S. Antimicrobial treatment for intensive care unit (ICU) infections including the role of the infectious disease specialist. Int J Antimicrob Agents 2007;29:494-500.  Back to cited text no. 3
    
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Williams A, Mathai AS, Phillips AS. Antibiotic prescription patterns at admission into a tertiary level intensive care unit in Northern India. J Pharm Bioallied Sci 2011;3:531-6.  Back to cited text no. 5
    
6.
Drupad HS, Nagabushan H, Prakash GM. Prospective and observational study of antimicrobial drug utilization in medical intensive care unit in a tertiary care teaching hospital. Int J Pharmacol Res 2016;6:13-7.  Back to cited text no. 6
    
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Hanssens Y, Ismaeil BB, Kamha AA, Elshafie SS, Adheir FS, Saleh TM, et al. Antibiotic prescribing pattern in a medical intensive care unit in Qatar. Saudi Med J 2005;26:1269-76.  Back to cited text no. 8
    
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Al Ansari A, Azizullah M, Khan JA, Lamine M. Antibiotic prescription patterns in an intensive care unit in the Kingdom of Bahrain: An observational prospective study. Med Sci 2013;2:371-4.  Back to cited text no. 9
    
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Malacarne P, Rossi C, Bertolini G; GiViTI Group. Antibiotic usage in intensive care units: A pharmaco-epidemiological multicentre study. J Antimicrob Chemother 2004;54:221-4.  Back to cited text no. 10
    
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Shankar PR, Partha P, Dubey AK, Mishra P, Deshpande VY. Intensive care unit drug utilization in a teaching hospital in Nepal. Kathmandu Univ Med J (KUMJ) 2005;3:130-7.  Back to cited text no. 11
    
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Ofori-Asenso R, Agyeman AA. Irrational use of medicines-A summary of key concepts. Pharmacy (Basel) 2016;4. pii: E35.  Back to cited text no. 12
    
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Goldstein EJ, Petrak RM, Sexton DJ, Butera ML, Tenenbaum MJ, MacGregor MC, et al. The value of an infectious diseases specialist. Clin Infect Dis 2003;36:1013-7.  Back to cited text no. 13
    
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Ohji G, Doi A, Yamamoto S, Iwata K. Is de-escalation of antimicrobials effective? A systematic review and meta-analysis. Int J Infect Dis 2016;49:71-9.  Back to cited text no. 14
    
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Harris AD, Perencevich E, Roghmann MC, Morris G, Kaye KS, Johnson JA. Risk factors for piperacillin-tazobactam-resistant Pseudomonas aeruginosa among hospitalized patients. Antimicrob Agents Chemother 2002;46:854-8.  Back to cited text no. 15
    
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Ventola CL. The antibiotic resistance crisis: Part 1: Causes and threats. P T 2015;40:277-83.  Back to cited text no. 16
    
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Schmitt S, McQuillen DP, Nahass R, Martinelli L, Rubin M, Schwebke K, et al. Infectious diseases specialty intervention is associated with decreased mortality and lower healthcare costs. Clin Infect Dis 2014;58:22-8.  Back to cited text no. 17
    
18.
Badar VA, Navale SB. Study of prescribing pattern of antimicrobial agents in medicine intensive care unit of a teaching hospital in central India. J Assoc Physicians India 2012;60:20-3.  Back to cited text no. 18
    
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Banerjee T, Anupurba S, Singh DK. Poor compliance with the antibiotic policy in the intensive care unit (ICU) of a tertiary care hospital in India. J Infect Dev Ctries 2013;7:994-8.  Back to cited text no. 19
    


    Figures

  [Figure 1], [Figure 2], [Figure 3], [Figure 4]
 
 
    Tables

  [Table 1], [Table 2], [Table 3]



 

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