INTRODUCTION
Antibiotics have transformed the practice of medicine, making once-lethal infections readily treatable and making other medical advances, such as cancer chemotherapy and organ transplants, possible. The misuse of antibiotics has also contributed to the growing problem of antibiotic resistance (AR), which has become one of the most serious and growing threats to public health.[1 2 3 4 5 , 6 Clostridium difficile infection. [7 , 8 , 9 10 , 11 12 , 13 , 14 , 15 , 16
METHODOLOGY
An interventional and cross-sectional study was carried out at a 17-bedded neurosurgery intensive care unit (ICU) of a tertiary healthcare teaching hospital in Northern India for the duration of 19 months, from September 2018 to April 2020. Study patients were all the patients admitted to the neurosurgery ICU during the study and who were on antimicrobials for more than 48 h and continued thereafter, were identified and recruited into the study. The study tool was an antibiotic prescription chart for pre and post-intervention phase [Figure 1 ] and postprescription review and feedback form for postintervention phase [Figure 2 ] that was used for data collection. The primary outcome of the study was days of therapy (DOT) per 1000 In-patient days (PD) for antimicrobials. Data analysis was done by SPSS 23 IBM (International Business Machines Corporation), Amonk, New York, United States, 2009. The following antimicrobials, administered intravenously, intramuscularly, or orally were included in the study: β-lactams, fluoroquinolones, aminoglycosides, metrogyl, β-lactam/β-lactamase inhibitor combinations, third-and fourth-generation cephalosporins, clarithromycin, clindamycin, carbapenems, linezolid, tigecycline, minocycline, colistin, teicoplanin, and vancomycin.
Figure 1: Antibiotic prescription chart. ICU: Intensive care unit
Figure 2: Postprescription review and feedback form
The whole study was divided into three parts – baseline or preintervention, intervention and postintervention phase. The baseline phase involved evaluation of antibiotic utilization and prescribing practices and appropriateness for the same without provision of any recommendations. During the intervention phase, a 3-component intervention was introduced, i.e. active ICU rounds, postprescription review with feedback and teaching programs. Postintervention phase involved evaluation of antibiotic utilization and prescribing practices and appropriateness for the same with provision of recommendations.
Data collection for baseline and postintervention period
The study tool was an antibiotic prescription chart for pre and postintervention phase [Figure 1 ] and postprescription review and feedback form for postintervention phase [Figure 2 ] that was used for data collection. Antibiotic prescription chart comprised of 2 sections. The first section documented the demographic details of patients, diagnosis, fever, total leucocyte counts, date of admission/discharge to ICU, date of surgery. The second section documented the indication for antibiotics, whether antibiotics were being prescribed for prophylaxis or definitive treatment, the dose, duration, start and stop date of antibiotic prescribed, microbiological culture and sensitivity results. Medical records of the patients were retrieved from the hospital information system.
Intervention
The misuse of antibiotics which was observed with the help of antibiotic prescription chart in baseline period, that needed improvement, thus interventions were planned accordingly. Intervention was in three component, first one was AS ward rounds, conducted on a daily basis during the postintervention period at the neurosurgery ICU by the infection control team (ICT). The following types of interventions were recommended during rounds by the ICT: To stop, continue, de-escalate, and modify the current prescribed antimicrobial therapy, to stop redundant cover and to change the route/dose/frequency of antimicrobial therapy. Second one was postprescription review with Feedback in which review of each antibiotic was done on days 3, 5, and 7 from the date of antibiotic initiation, to assess the appropriateness of antibiotics and to give recommendations and check compliance for the same. The final decision to act on the recommendations was left to the treating consultant. Third intervention was teaching and training programs, to disseminate information regarding AS.
Outcome measures
Our primary outcome measure was DOT per 1000 in-patient days (PD) for antimicrobials. In this study, One DOT represents the administration of a single agent on a given day regardless of the number of doses administered or dosage strength. PD were calculated by counting the number of patients present in any given location (Hospital or Ward) at a single time point during a 24-h period.
DOT per 1000 in-patient days = DOT/In-patient days × 1000.
Our secondary outcome measures were proportion of prescriptions with inappropriate use of antibiotic and cost of antibiotics per patient day. Our process measures include: rates of de-escalation, intervention rate and acceptance rate for recommendations on the prescriptions with inappropriate use of antibiotics during postintervention phase. Patient-specific outcomes were average length of stay and mortality rate in ICU. The prevalence of multi-drug-resistant organisms (MDROs) such as methicillin-resistant Staphylococcus aureus (MRSA), carbapenem-resistant Enterobacteriaceae , vancomycin resistant Enterococci (VRE), were also assessed. Data analysis was done using Microsoft excels and SPSS 23.
OBSERVATIONS AND RESULTS
Demographic and clinical characteristics
During the baseline or preintervention phase, a total of 152 patients were recruited for the study. Similarly, 166 were recruited during the postintervention phase [Table 1 ].
Table 1: Clinical characteristics of patients during pre- and post-intervention phase
Primary outcome measures: Days of therapy per 1000 in-patient days
The primary outcome, DOT per 1000 In-patient days for study antimicrobials in the preintervention phase and postintervention phase was 2123.81 and 1743.82, respectively. Overall decrease in the DOT per 1000 In-patient days from preintervention to postintervention phase was 17.8% (P = 0.35). Antibiotic use was significantly lower in the intervention phase for 3rd generation cephalosporins, aminoglycosides, metrogyl, vancomycin, colistin, carbapenems, clarithromycin, linezolid, minocycline, and fluoroquinolones. The use of β-lactam/β-lactamase inhibitor combinations, clindamycin and teicoplanin increased in the intervention group [Figure 3 ]. The average duration of antibiotics was maximum for colistin, i.e.,14.3 days and minimum for cefuroxime, i.e. 4 days in preintervention phase. The average duration of antibiotics was maximum for vancomycin, i.e. 10.5 days and minimum for cefuroxime, i.e. 3.7 days in postintervention phase.
Figure 3: Comparison of DOT/1000 in-patient days of antibiotics during pre- and post-Intervention phase. DOT: Days of therapy
Secondary outcome measures
Proportions of prescriptions with inappropriate use of antibiotics during postintervention phase
The decrease rate in the number of prescriptions with inappropriate use of antibiotics was 18.4% (P = 0.31) [Figure 4 ].
Figure 4: Total number of prescriptions with inappropriate use of antibiotics during pre- and post-intervention phase
The most frequently observed causes for inappropriate use of antibiotics during postintervention phase, as observed were; absence of clinical indication (CI), pathogen-antibiotic mismatch (PA), unnecessary double coverage of antibiotics (DC), antibiotic was prescribed at a wrong dose, wrong route, and/or wrong frequency or use of broad-spectrum antibiotics (BS) [Table 2 ].
Table 2: Number of different types of prescriptions with inappropriate use of antibiotics on day 3, day 5, and day 7 of antibiotic initiation during postintervention phase
The total number of recommendations was made on the prescriptions with inappropriate use of antibiotics during postintervention phase were 545 in number. Out of which only 175 recommendations were accepted and 370 recommendations were not accepted. Hence, Acceptance rate for recommendations on the prescriptions with inappropriate use of antibiotics during postintervention phase was 32% [Figure 5 ].
Figure 5: Number of recommendations which were accepted on day 3, day 5, and day 7 of antibiotic initiation during postintervention phase
The acceptance rate or compliance rate for recommendations on the prescriptions with inappropriate use of antibiotics on day 3, day 5, and day 7 of antibiotic initiation during postintervention phase were 21.7%, 39.5%, and 35.4%, respectively and different types of recommendations which were made on the prescriptions with inappropriate use were, to modify the prescribed antimicrobial therapy, to continue the prescribed antimicrobial therapy, to stop redundant cover (R), to stop the current prescribed antimicrobial therapy, to de-escalate the prescribed antimicrobial therapy or/and to change the route, dose, frequency [Tables 3 and 4 ].
Table 3: The total number of different types of recommendations and their acceptance rate which were made on the prescriptions with inappropriate use of antibiotics on day 3, day 5, and day 7 of antibiotic initiation during postintervention phase
Table 4: Total number of different types of recommendations and their acceptance rate on day 3, day 5, and day 7 of antibiotic initiation during postintervention phase
Cost of antibiotic usage per patient day
The cost of antibiotic usage per patient day during pre- and post-intervention phase was INR 257.01 and 178.91, respectively. The reduction in cost of antibiotic usage per patient day from pre to post-intervention phase was INR 78.1. The rate of reduction of cost of antibiotic usage per patient day from pre- to post-intervention phase was 30.8% (P = 0.59).
Process measures
Rates of de-escalation according to culture susceptibility, total leukocyte counts and clinical evaluation: During postintervention phase rate of de-escalation according to culture susceptibility, total leukocyte counts and clinical evaluation were 7.6% and 23.2%, respectively
Intervention Rate: There were 296 number of courses of therapy in which modification is recommended. Moreover, the total number of courses were 512. Hece, the intervention rate in postintervention phase was 57.8%
Acceptance Rate: Acceptance rate for recommendations on the prescriptions with inappropriate use of antibiotics on day 3, day 5, and day 7 of antibiotic initiation during postintervention phase was 32%.
Patient-specific outcomes
Average length of stay in ICU: The average length of stay in the ICU during pre- and post-intervention phase was 11.7 days and 12.8 days, respectively
Mortality rate in ICU: The mortality rate in the ICU during pre and post intervention phase was 4.60% and 7.69%, respectively.
Microbiology profile
The prevalence of MDROs: The overall prevalence of MDROs included in the study (MRSA) and VRE) were 12.7% and 8.0% in the pre- and post- intervention phase, respectively. Organism with the highest prevalence was VRE [Figures 6 and 7 ].
Figure 6: Culture sensitivity versus antibiotic usage during preintervention phase
Figure 7: Culture sensitivity versus antibiotic usage during postintervention phase
It was concluded from species-specific distribution and antibiotic susceptibility pattern of all bacterial isolates recovered from all samples during preintervention phase that there was complete resistance to third-generations cephalosporins, sensitivity of Pseudomonas species was <50% to carbapenems group of antibiotics, Acinetobacter baumanii was 100% resistance to carbapenems, 100% susceptibility to colistin and Fosfomycin and 100% susceptibility to vancomycin and teicoplanin to Gram-positive bacterial isolates. During postintervention phase, there was 97% resistance to third-generations cephalosporins, Pseudomonas species was 100% resistance to carbapenems, Acinetobacter baumanii was 95% resistance to carbapenems, 100% susceptibility to colistin and fosfomycin except Proteus Mirabilis isolates and 87.5% susceptibility to vancomycin and teicoplanin to Gram-positive bacterial isolates.
DISCUSSION
There has been an increasing number of studies that have evaluated the clinical and economic impact of antibiotic stewardship programs (ASPs) in the last few years.[17 et al . reported reduction in DOT per 1000 in-patient days from baseline to intervention phase, i.e. 1201.7–987.9.[18 19 , 20 , 21 , 22 23 et al . reported 4.3% decrease in overall antibiotic utilization rates from baseline to stewardship period in neonatal ICU (NICU).[24 et al . stated that the efficacy of AS day 3 audit-and-feedback program was confirmed by the 21% reduction in targeted antibiotic use among patients qualifying for the intervention.[25 et al . reported a 25% increase in the antibiotic use after implementation of such interventions in a 948-bed university hospital in the Netherlands.[26
The use of β-lactam/β-lactamase inhibitor combinations, clindamycin, and teicoplanin increased in the intervention group compared to the baseline group and we attribute this change due to the de-escalation from the carbapenems and polymyxins. We noted a marked decrease in the use of restricted antibiotics such as carbapenems, colistin, and vancomycin which was similarly reported in other studies.[27 , 28 et al . reported the decrease in ampicillin and vancomycin utilization rates from baseline to stewardship period in NICU were 12.8% and 35.5%, respectively. And increase in the clindamycin utilization rates from baseline to stewardship period in NICU was 20.8%.[24 et al . analysed results from 3 years preintervention and 7 years postintervention, and documented a reduction in use of third-generation cephalosporins and aztreonam and a stable rate of use of fluoroquinolones and imipenem when ID physician and clinical pharmacist monitored prescription of BS antimicrobials and gave feedback to prescribers.[29
Reduction in the average duration of antibiotics from preintervention to postintervention phase was due to frequent monitoring by ICT which facilitate the reassessment of antibiotic therapy and may result in facilitation of de-escalation or termination of antibiotic therapy. Manuel et al . showed that antimicrobial intervention is associated with a shorter duration of antibiotic therapy, regardless of changes in antimicrobial consumption.[30 et al . reported a reduction in and mean duration of prophylactic antibiotics.[31
We found that 49% of prescriptions were with inappropriate use of antibiotics, which is higher than the 30% rate reported in studies conducted in high-income settings.[32 33 et al . reported that 70% of the total antibiotic prescriptions were inappropriate which is higher than our study.[18
Reassessment of antibiotic prescriptions approximately every 3 days after administration has been shown to be effective for optimizing empirical therapy (day 3 bundle).[34 32
There were many reasons for low acceptance rate for recommendations on the prescriptions with inappropriate use of antibiotics during postintervention phase, that were resistance of primary treating consultant towards acceptance of recommendations, significant delays in reviewing the antibiotic feedback forms, absence of interaction with the primary treating consultant within an actionable time frame after feedback, and lack of monitoring of compliance with feedback and duration of therapy. This signals that messaging in stewardship is important and is consistent with stewardship literature[35 et al . observed that compliance with ASP recommendations was 54% during the implementation period.[21 et al . reported that the acceptance rate for ASP recommendations was 60.7%[18 36 , 37 et al . reported increase in appropriate antibiotic prescribing in urology patients from 38% to 89%, following an introduction of an antibiotic prescription chart.[31 et al . reported that acceptance rate of different types of recommendations which were made on the prescriptions with inappropriate use of antibiotics during intervention phase such as de-escalation, discontinue, unnecessary DC, continue the same and modify according to susceptibility were 42.2, 44.3, 64.5, 94.1, and 22.2 (in percentage), respectively, which is higher than our study.[18
Active dialogue and constant interaction with the in-house ICU staff and primary treating team along with active ICU rounds by the ICT (to monitor the patient's progress after the recommendations were given) seemed to ensure better acceptance. Dialogue and discussion between the ICT and the ICU staff were necessary to establish trust and rapport. Moreover, ICT took the opportunity to educate staff about and create awareness of the ASP. Overall, we found that prospective audits and feedback in the intervention phase reduced antibiotic utilization during postintervention phase.
The rate of reduction in the cost of antibiotic usage per patient day from preintervention to postintervention phase was 30.8%. Malani et al . reported that implementation of ASP was associated with a 13.3% decrease in antimicrobial cost per patient day.[38 et al . reported in a before-and-after study that the implementation of AS for improvement of the timeliness of switch to oral antimicrobials reduces antimicrobial costs without changing the length of hospital stay.[39 et al . observed that there was a decrease in mean monthly cost of consumption of restricted antimicrobials on evaluation of multidisciplinary ASP. Moreover, the savings were all transferred to patients because the predominant patient population pays “out of pocket.”[21
Rates of de-escalation according to culture susceptibility, total leukocyte counts and clinical evaluation was 7.6% and 23.2%, respectively, this is low due to reluctance of primary treating consultant to accept recommendations which were made on the prescriptions and habit of using BS antibiotics to give maximum coverage. Rupali et al . reported that the rate of de-escalation according to culture susceptibility was significantly higher in the intervention group compared to the baseline group, i.e. 42.7% versus 23.6%, suggesting a definite trend with regard to the judicious use of antibiotics.[18 33
The intervention rate in postintervention phase in this study was low as compared to other studies. A study of evaluation of postprescription review and feedback reported intervention rate of 70.3%, due to high rate of prescriptions with inappropriate use of antibiotics.[18
The acceptance rate for recommendations during postintervention phase was 32%, an intervention of 5 months is too limited a period of time to impact acceptance rates significantly. A study of evaluation of postprescription review and feedback reported acceptance rate of 60.7%.[18
Although our study intervention led to decreased antimicrobial use, there was no significant survival benefit.
The organism with the highest prevalence was VRE in both the phases is likely due to the use of restrictive antibiotics such as vancomycin. There was a significant reduction in the use of vancomycin with our intervention probably because the VRE infection rates were low in postintervention phase. Rupali et al . reported that the prevalence of MDROs was almost 30% across all phases of the study.[18
CONCLUSION
Based on the observations and discussion, this can be concluded that AR in both health care and community settings represents a daunting challenge. AS can provide all practitioners with tools to prevent the overuse of valuable resources and help control the increase in AR.
Recommendation
Based on observations and findings, an evidence-based antibiotic prescription policy should be implemented in neurosurgery ICU. Regular review and feedback of antibiotic usage are necessary to avoid excess consumption of antibiotics. Teaching and training of AS for all the stakeholders in the hospital should be on priority basis.
Financial support and sponsorship
Nil.
Conflicts of interest
There are no conflicts of interest.
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