key: cord-1044966-i7q4xqe5 authors: O’Kelly, B.; Rueda-Benito, A.; O’Regan, M.; Finan, K. title: An audit of community acquired pneumonia (CAP) antimicrobial compliance using an intervention bundle in an Irish hospital date: 2020-08-12 journal: J Glob Antimicrob Resist DOI: 10.1016/j.jgar.2020.07.021 sha: 407f2c556a6bca66463fd51f0e88a5d4dd35e50d doc_id: 1044966 cord_uid: i7q4xqe5 BACKGROUND: Hospitalisations with community acquired pneumonia (CAP) are often not managed in accordance with antimicrobial guidelines. AIM: The aim of this study was to assess if guideline driven antimicrobial prescribing for CAP can be improved using an intervention bundle. Secondary measures assessed were length of stay (LOS), mortality, duration of intravenous antibiotics and total antibiotic duration, improving uptake of appropriate investigations and documentation of CURB65. METHODS: A retrospective cohort of hospitalised CAP patients from August -September 2018 was compared with a post intervention prospective cohort from May-June 2019. Intervention bundle included a mobile audience response session (MARS) session, promotion of the antimicrobial app, development of a physical card with local guidelines and incorporating CURB65 into the unscheduled admission proforma. Local guidelines are in keeping with the British Thoracic Society (BTS) CAP guidelines. RESULTS: 69 adult patients (>18 years old) were included in the study (37 retrospective, 32 prospective). Overall compliance with local CAP guidelines improved from 21% to 62.5% (p < 0.001). No difference in initial intravenous antibiotic duration was seen, median 4 vs 4 days (p = 0.73), total antibiotic duration was significantly shorter in the post intervention group, median 9 vs 7 days (p = 0.01). No difference in length of stay or mortality was seen between the groups. Documentation of CURB65 improved from 5.6% to 46.9% (p < 0.01). Uptake of streptococcal urinary antigen improved from 18.9% to 40.6% (p = 0.024). CONCLUSION: A simple low cost quality improvement bundle can significantly increase appropriate antimicrobial prescribing and shorten total duration of antibiotics. (DALYs) and fourth for deaths [1] . In Europe there are approximately 1 million community acquired pneumonia admissions per year (European Lung Whitebook) [2] . Admission rates per country vary widely. Ireland has the highest rate of admissions with 227.24 per 100,000, which account for 4.5% of unscheduled hospitalisations annually. A cost analysis in a single tertiary centre has shown that mean cost per stay is €14,802 in 2017 [3] . The decision to admit and antimicrobial choice for CAP has been highly protocolised based on the well validated scoring systems including CURB65 for patients presenting to hospitals [4, 5] . Despite this, documentation of severity scores for unscheduled admissions has been poor [6] [7] [8] [9] [10] . Patients with low CURB65 scores are admitted unnecessarily [11] . Admitted patients tend to be under-investigated [12, 13] . Similarly, antimicrobial use is poorly compliant with BTS guidelines and has been overly broad in spectrum of activity [14, 15] . Length of stay and overall antibiotic duration have been shown to be prolonged in some cases [3] . The aim of this audit was to assess if an intervention bundle featuring a single interactive teaching session using a mobile audience response system (MARS)with the adjunctive measures of promoting the antimicrobial mobile app, providing a physical card containing guidelines, and integrating CURB65 score into to the medical admission proforma could improve antimicrobial stewardship of in-hospital CAP. Secondary outcomes reviewed were length of stay (LOS), uptake of appropriate investigations, and time to antibiotics in the prospective group. This audit was an initiative of the Sligo University Hospital (SUH) antimicrobial stewardship committee in conjunction with the respiratory department. Community acquired pneumonia management was identified as an area of particularly poor compliance. This was evident from preliminary data from a hospital wide pharmacy audit of overall prescription within the hospital. SUH is a 359-bed hospital in Ireland with a 24-hour emergency department (ED). Data collection for the J o u r n a l P r e -p r o o f retrospective part of the study was from August 1 st 2018 to September Compliance with antimicrobial guidelines was defined as correct route, dose and frequency. If additional antibiotics were given despite otherwise complete adherence the episode was deemed non adherence. For example, for a patient with CURB65 of 3; co-amoxiclav 1.2g eight-hourly intravenously (IV) + clarithromycin 500mg twelve hourly per orally (PO) with additional gentamicin 5mg/kg once daily (OD) IV would be deemed non adherence due to presence of gentamicin despite correct prescription otherwise. The 'intervention bundle' was undertaken at the beginning of non-consultant hospital doctor (NCHD) 'changeover', a period when junior doctors change roles within a hospital or J o u r n a l P r e -p r o o f between hospitals to gain experience in a new specialty in a period of training prior to sub-specialisation, in early April 2019. Four low cost measures were implemented in the bundle: Firstly an interactive presentation was given during a 1-hour medical Grand Rounds session using online Mentimeter® software, a MARS. This session was also given to the ED separately. Assessment of knowledge of correct antimicrobial choice based on CURB65 score was assessed at the beginning and end of each presentation through collective voting using smartphones with real time data projected onto the presentation. Data are also automatically collated in Microsoft® Excel format. Common pathogens, appropriate investigations, rationale of antimicrobial choice, antimicrobial resistance, and results of retrospective audit were presented. Secondly, the local SUH antimicrobial SHARx smartphone application for iOS and Android was also promoted. This app is password protected and was developed by MEG Support Tools with a grant from Pfizer Healthcare Ireland, the content of the app is solely an electronic extension of local antimicrobial guidelines, which are decided upon by the antimicrobial stewardship committee. Thirdly an 85x55mm card with CURB65, appropriate investigations and a table of local guidelines was given to all medical and ED faculty members present at the presentations (appendix 1). The cards are the same size as a standard hospital swipe card and were intended to slide behind swipe cards on hospital lanyards. Cards were also left in the morning medical handover meeting room. Lastly, the CURB65 criteria was also added to the admission proforma for unscheduled patients admitted through ED. Patients with CAP between May and June 2019 were identified using the same methodology and inclusion/exclusion criteria as the retrospective audit. Door to needle time for antibiotics was recorded at this time as a potential variable for future audit. NCHDs were not explicitly informed their practice subsequent to the intervention would be audited as part of a re-audit. Data was compiled on Microsoft Excel 2019® and statistical analysis was performed on IBM® SPSS® Statistics V26.0. Chi-squared testing was used for categorical data. Mann-Whitney U testing was performed on non-normally distributed nominal data (length of stay, duration J o u r n a l P r e -p r o o f of antibiotics). Kruskal-Wallis testing was used for non-normally distributed ordinal/nominal data related to a scale i.e. time to antibiotics for given CURB65 score. Ethical approval was not sought as this study was performed in audit format and used standard clinical data. The audit was registered with the local Clinical Audit Office in SUH and was in line with local clinical audit and data protection requirements. Sixty-nine patients were included in the final study (37 pre-intervention, 32 post-intervention). Twentysix patients were excluded as they were either miscoded as CAP and had other diagnoses, many of which were HAP (15 pre-intervention, 11 post-intervention). Some patients had missing charts and thus incomplete data. Of 69, thirty-seven (53.6%) patients were female with a mean age of 74.8 years (SD ±16.08). Eleven (15.9%) were nursing home residents. Mean CURB65 was 2.16 (SD±1.17), 50 patients had a CURB65 of 2 or more ( Figure 1 ). Twenty-eight (40.6%) of patients had a previous respiratory diagnosis. Chronic Obstructive Pulmonary Disease (COPD) was the most common single comorbidity (23%). Median White cell count (WCC) and C-reactive protein (CRP) were 11x10 9 cells/ml and 70 mg/L (Table 2) . Median LOS was 4 days (pre-intervention IQR (3-7), post-intervention IQR (3-11)), there was no significant difference between pre and post intervention groups. Two deaths occurred in the pre intervention group and three in the post intervention group 5.5% vs 9.3%, this proportion of deaths between groups was not significant, p=0.53. All patients who died had a CURB65 of 3 or more and documented respiratory sepsis (Table 3) . Regarding the interactive medical grand rounds teaching session, 25 NCHDs engaged on the day of the intervention. Amoxicillin and clarithromycin were correctly identified as the antibiotic of choice for a patient with CURB65 of 2 at the start of the session by 15/25 (60%). In the independent teaching session with ED doctors, of seven present on the day of the session, three (42.9%) correctly identified J o u r n a l P r e -p r o o f the appropriate antimicrobial choice for CURB65 of 2. At the end of session re-assessment this increased to 21/25 (84%) medical doctors and 7/7 (100%) for ED doctors. Medical doctors rated their perceived diagnostic accuracy of chest radiograph findings for pneumonia compared to a consultant radiologist at 68%, ED doctors rated their accuracy at 64%. On review of admission notes there was 81% concordance of documented findings with official radiology reporting. Streptococcus pneumoniae was known to be the most common cause of CAP in 84% of medical doctors and 100% of ED doctors. Streptococcus pneumoniae was the most common causative organism identified, n=4. (Table 4 ). Intravenous antibiotics were received by 92% of patients. Co-amoxiclav was the most common antibiotics used, n=41 (61.2%). Clarithromycin was the second most common, n= 34 (49.3%) ( Table 5 ). Systemic inflammatory response score (SIRS) was 2 or more in 34 patients, indicating possible respiratory sepsis (SIRS: Temperature >38 or <36°C, heart rate >90 beats/minute, tachypnoea >22 breaths/minute, WCC >12 or <4*10 9 cells/L, any criterion fulfilled scores one point, two or more points indicate possible sepsis). Documentation of SIRS score was done in 10 of 69 (14.5%) patients. Retrospective audit: Overall compliance with guidelines was 21%. The largest contributing factors for this was over-use of co-amoxiclav and use of unnecessary antibiotics for CAP like piperacillintazobactam and gentamicin (Table 5) . Prospective audit: A statistically significant increased uptake of pneumococcal urinary antigen was seen, 19% pre-intervention group to 41% in post-intervention group (p= 0.024). No difference was seen for other investigations (blood cultures, legionella antigen detection, sputum cultures). An increase was documentation was seen for CURB65 4.5% vs 46.9% p<.001. Overall compliance improved to 62.5% (beta-lactam/lactamase compliance 21/30 70%, clarithromycin 19/25 77.7%), p<.001 (Table 3) . One dose of piperacillin-tazobactam was administered in ED prior to switch to appropriate antimicrobials, this was included as an episode of non-adherence to guidelines. Appropriate use of amoxicillin increased from a single patient who received IV therapy in the retrospective part of the audit to six J o u r n a l P r e -p r o o f patients in the prospective, four receiving oral amoxicillin and two IV, one of whom had documented sepsis and another with a SIRS score of 2. No difference was seen in total duration of IV antibiotics mean 4(IQR 2-4.5) days vs 4(IQR 2-5) days, p= 0.70. A difference was seen in total antibiotic duration pre intervention median days 9(IQR 7-11) vs post intervention 7 (IQR 6.5-9) days, p=0.01. Mean time to antibiotics in the prospective audit was 142 minutes. Kruskal-Wallis analysis showed a statistically significant association between time to antibiotics and CURB65 score, p=0.023 (Figure 2 ). In this study we have observed an improvement in stewardship practices for patients with CAP in association with a combination of interventions that included an interactive teaching session, reminder cards, promotion of a prescribing app, and addition of CURB65 to the admission pro forma. Use of an educational session while improving access to guidelines using a pocket book has also been shown to significantly deescalate antimicrobials and decrease length of stay in a cohort of post-operative patients in the Netherlands [17] . Learning using MARS are a rising and viable pedagogical technique in the undergraduate medical domain [18] . Audience response systems have extended into teaching in clinical practice in small studies with some positive impact [19, 20] . Other strategies within the bundle focused on increasing ease of access to the guidelines; the Sharx mobile app was promoted which has recommendations on investigations, CURB65 and antimicrobials. The hard copy card was designed to slide into a hospital card holder on a lanyard to give those that do not have a smartphone or choose not to use the app the same level of access to CAP guidelines when assessing CAP patients. Our study showed that at baseline hospital doctors had some understanding of antimicrobial choice for CURB65 (60% medicine, 42% ED) but this was not reflected in antimicrobial choice in practice (21% compliance). Reasons for this may be many-fold and give rise to questions about doctor's belief in J o u r n a l P r e -p r o o f effectiveness of scoring systems to dictate management of CAP, mismatches between perceived effectiveness of guideline-based treatment and perceived unwellness of their patients, or complex behavioural factors around prescribing antibiotics. Studies examining the behavioural practices of healthcare professionals (HCPs) around antibiotic prescribing have been done. Thematic analysis of qualitative interviewing of HCPs has shown prescribing can be dominated by culture rules which dictate a 'prescribing etiquette'. In essence, senior decision makers are more likely to prescribe based on personal experience than on policy, junior members are unlikely to challenge these decisions and overall members within the group are less likely to interfere with antimicrobial decisions of their peers [21] . Effective antimicrobial stewardship quality improvement strategies should take these factors into consideration and adopt previously validated, evidence based methods of behavioural and social sciences to implement behaviour change to foster true sustainability of stewardship strategies [22] . The recognition of the importance of this issue is gaining traction and an international Working Group of the Joint Programming Initiative on Antimicrobial Resistance (JPIAMR) have released a consensus paper defining key research areas where behavioural science can optimize antimicrobial stewardship programmes [23] . In this study the most problematic areas were over-prescription of co-amoxiclav where amoxicillin would have been adequate, and the unnecessary use of gentamicin and the anti-pseudomonal penicillin piperacillin-tazobactam. This directly correlated with CURB65 score. All four patients with a CURB65 score of four received piperacillin-tazobactam (Table 6 ). High levels of overuse of piperacillintazobactam has been described in another Irish study [6] . Documentation of CURB65 was poor at just 5.6%, and low levels of investigations (19% pneumococcal urinary antigens, 19% sputum cultures) were also seen in the retrospective audit and has been described elsewhere [12, 13] . In the prospective study overall compliance increased to 62%. Although individual compliance with beta-lactams and clarithromycin improved to higher percentages (70%, 77%), the combined compliance was necessary to qualify as a compliant episode (Table 3) . Increasing compliance of antibiotics in CAP with care bundles has had mixed results. A national UK BTS audit improved compliance from 25% to 29.4% [24] . A smaller study implementing a bundle over 18 months had more J o u r n a l P r e -p r o o f success, documentation of CURB65 increased from 32% to 94%, antibiotics prescribing improved from 48% to 87%. High levels of success were attributed to the perseverance of the multidisciplinary team wo had weekly meetings and used a weekly compliance surveillance tool [25] . Areas of improvement in our bundle were the near elimination of piperacillin-tazobactam from use bar one dose in ED, elimination of gentamicin and rise in use of amoxicillin for CURB65 0-2. Although, this remained the single largest problem area with eight patients in the prospective group receiving co-amoxiclav in place of amoxicillin for CURB65 0-2 ( Table 6) . No impact on duration of IV antibiotics was seen (median 4 vs 4 days), this may reflect the ongoing necessity for IVs in the early phase of treatment in both groups as 49.3% of patients had markers for sepsis (SIRS ≥2). A decrease in total antibiotic duration was seen due to shortened periods of oral antibiotics both in hospital and prescribed at discharge (median total antibiotics duration 9 vs 7 days p=0.01) ( Table 3 ). An organism was identified in 16% of patients. CAP has traditionally been poorly differentiated in terms of causative organism [26] . As PCR of respiratory samples was not performed the profile of organisms identified in the study are unlikely to be fully representative of causes of CAP. Streptococcus pneumoniae was the most common organism identified which is unsurprising at it is the single largest bacterial pathogen representing 17.7% of all CAP internationally [27] . Gram negative organisms (Pseudomonas aeruginosa, Haemophilus influenzae, Moraxella catarrhalis, and E. coli) were the largest group identified (Table 4 ). A significant proportion of patients had chronic respiratory diagnoses, cognizance of the profile of possible organisms that can cause pneumonia in this patient group is important to direct therapy should initial CAP therapy fail, this has been described elsewhere [28] . Time to antibiotics in the prospective study showed significant reduction in time for each CURB65 score, as less than 50% of CURB65 scores were documented, and less so for SIRS and sepsis, time to antibiotics was likely driven by identification of these markers without their documentation (Figure 2 ). This study has significant limitations. Sample size is small given the frequency of presentations of unscheduled CAP admissions. Seasonality does influence rate of CAP hospitalizations, with more admissions occurring during the winter season [29, 30] . Although both retrospective and prospective parts of the study were outside of the winter season, they were not at the same time of year (August/Septemberretrospective, May/Juneprospective). Consultants and registrars were the same throughout both periods, but more junior firm members, interns and senior house officers, may have been different due to the rotation cycles of trainees. The prospective audit was performed just after the April 'changeover' so all NCHDs in the hospital would be the same for the duration of the prospective period. Also having only two time points of assessment i.e. before and after the interventional teaching session, means confounders may be present and it is difficult to confirm what extent the improvements were due to the intervention bundle. Assessment on a continuous basis, as seen with quality improvement design would have aided in differentiating the relative advantages from the individual aspects of the bundle. It would also have indicated the sustainability of the intervention bundle. As mentioned in the methodology section, local guidelines at SUH are in line with BTS CAP guidelines first published in 2010 [14] . With the release of NICE CAP guidelines in 2014, BTS released annotated guidelines mostly highlighting high levels of overlap between NICE and BTS including the use of amoxicillin for low severity pneumonia, amoxicillin plus a macrolide for moderate severity, and betalactam/beta-lactamase-inhibitor plus a macrolide for patients with severe disease (all in patients without penicillin hypersensitivity) [31] . Antimicrobial choice for CAP has not changed significantly over time. One reason for this is the modest increase in antimicrobial resistance of common CAP organisms. The SENTRY Antimicrobial Surveillance Program identified 19,123 isolates of S. pneumoniae in Europe between 1997-2016 and found isolates were generally susceptible to penicillins and had a small rise in resistance over that time-frame [32] . Similarly invasive pneumococcal disease (IPD) with penicillin non-susceptibility in the UK reported to the European Centre of Disease Control (ECDC) in 2010 was 3.1% (95%CI 2-4), this rose to 5.6% (95%CI 5-6) by 2018 [33, 34] . In essence CAP guidelines have not needed to change significantly. In the context of the current COVID-19 pandemic, the cause of infection in patients presenting to EDs with acute respiratory illnesses is obscured. Management of these patients can be more difficult to navigate for physicians as CAP and COVID-19 have many of the same features; cough, fever, hypoxia, infiltrates on radiograph and raised CRP. Commencing antimicrobials can be the reflex action and clinical cohorts of hospitalised COVID-19 patients show antimicrobial use can be as high as 95% [35] . Recently, NICE published guidelines for antimicrobial prescribing of CAP during the COVID-19 pandemic and offer guidance on investigations to differentiate bacterial pneumonia and COVID-19 [36] . Co-amoxiclav, doxycycline and levofloxacin are first-line antimicrobials for moderate to severe disease as per these guidelines. The authors of this manuscript caution the use of antimicrobials and recommend continuously reviewing the decision to continue antibiotics in patients who have COVID-19. Huttner et al offer guidance on this issue, recommending antibiotics only in severely unwell patients with hypoxia with a diagnosis of COVID-19 [37] . In this study we have shown that a simple low-cost intervention bundle using a MARS, and improving ease of access to CAP guidelines is associated with a significant improvement in antimicrobial stewardship practices. An increase in appropriate investigations, correct antibiotic choice and reduction in total length of antibiotics was seen. There was no impact on LOS, days of IV antibiotics, or mortality. Elements of this intervention bundle should be considered in larger better resourced quality improvement strategies for management of CAP. The authors have received no funding for this study. There are no conflicts of interest to report. Not required. Right 36 19 17 Left 20 11 9 bilateral 13 7 6 NHnursing home, COPDchronic obstructive pulmonary disease, ILDinterstitial lung disease, TBmycobacterium tuberculosis, HTNhypertension, IHDischaemic heart disease, CCFcongestive cardiac failure, CKDchronic kidney disease, T2DMtype 2 diabetes mellitus, CRP -C-reactive protein, WCCwhite cell count. α includes percutaneous coronary intervention, coronary artery bypass grafting, myocardial infarction. β includes prostate cancer, Mantle Cell Lymphoma, colorectal cancer, oesophageal cancer, breast cancer, renal cell carcinoma and lung cancer. 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Clinical Microbiology and Infection We would like to thank the medical and emergency faculties for engaging in this study and patients and their families without whom this study would not be possible. A physical card displaying this guideline was distributed. Dimensions allow it to slide behind an ID card holder Blue boxes indicate a non-compliance with the guidelines. Ceftriaxone was used in one case with CAP as a secondary diagnosis with intra-abdominal infection as the primary diagnosis, this was deemed appropriate in that setting. No other episodes had apparent underlying factors that account for deviation from guidelines.