Sepsis Education Initiative Targeting qSOFA.7

Sepsis Education Initiative Targeting qSOFA Screening for Non-ICU Patients to Improve Sepsis Recognition and Time to Treatment Kim Raines, DNP, RN, CRNP, AGACNP-BC, CCRN; Ronaldo A. Sevilla Berrios, MD; Jane Guttendorf, DNP, RN, CRNP, ACNP-BC, CCRN Downloaded from https://journals.lww.com/jncqjournal by BhDMf5ePHKav1zEoum1tQfN4a+kJLhEZgbsIHo4XMi0hCywCX1AWnYQp/IlQrHD3TDbD+Y6NAIFSoahMi+ihjEWE0UIvGmlJzJ6GmEH+4uI= on 11/06/2019 ABSTRACT Background: The quick-Sequential Organ Failure Assessment (qSOFA) criteria are recommended for iden- tifying non–intensive care unit (ICU) patients at risk for sepsis but are underutilized. Local Problem: We hypothesized that education on recognizing sepsis using qSOFA criteria and empower- ing nurses to trigger rapid response team (RRT) calls based on positive qSOFA scores would reduce time to recognition and time to intervention and improve treatment compliance in non–ICU patients. Methods: The methods involved a descriptive retrospective review of 60 sepsis patients (30 pre- and 30 posteducation) to determine sepsis recognition time (qSOFA-to-RRT); time-to-sepsis interventions (reported as median [interquartile range] hours); and percent compliance with interventions. Interventions: We provided qSOFA and sepsis education to more than 1000 nurses, physicians, and ad- vanced practice providers in a large tertiary hospital. Results: Posteducation, time to recognition (qSOFA-to-RRT) improved from 11.8 hours (3.4, 34.3) pre to 1.7 (0, 11.7) post (P = .005). Time from qSOFA to antibiotics improved from 1.4 hours (2.4, 6.2) pre to −4.7 (−25.4, 1.8) hours post (P < .01). Using qSOFA, compliance improved for antibiotics from 60% pre to 87% post (P = .02). Keywords: antibacterial agents, organ dysfunction scores, quick-Sequential Organ Failure Assessment (qSOFA) criteria, sepsis, sepsis education Sepsis is a life-threatening, medical emer- of them agree that a high proportion of patients gency and a leading cause of inhospital are not initially treated in the ICUs.1,2 Non-ICU mortality. The number of sepsis patients who nurses should be able to recognize signs of early are treated in the medicine ward range from 33% sepsis and organ dysfunction in order to trigger to 45% according to different authors, but all early treatment. In 1 study, 57.4% of rapid response team (RRT) patients had sepsis.3 Thus, Author Affiliations: Department of Critical Care Medicine, UPMC RRT providers, including hospitalists and ad- Hamot, Erie, Pennsylvania (Drs Raines and Sevilla Berrios); and vanced practice providers (APPs), are responsible Department of Acute/Tertiary Care, University of Pittsburgh School of for recognizing and treating sepsis in more than Nursing, Pittsburgh, Pennsylvania (Drs Raines and Guttendorf). half of all RRT activations. Timeliness of RRT notification in patients with sepsis is critical, as The authors thank Tim Cooney, MS, for performing the statistical delays in sepsis recognition and RRT activation analyses and Lisa Hurst, BSN, RN, CCRN, for assisting with delivery beyond 1 hour after meeting sepsis criteria of sepsis education. are independently associated with increased 30-day mortality, hospital mortality, and hospi- Supplemental digital content is available for this article. Direct URL tal length of stay.4 Septic shock occurs late in the citations appear in the printed text and are provided in the HTML and continuum with mortality exceeding 40%.5 PDF versions of this article on the journal’s Web site (www.jncqjournal.com). One large multicenter sepsis quality improve- ment (QI) project conducted in 60 academic and The authors declare no conflicts of interest. community hospitals across the United States evaluated outcomes for patients with sepsis. Correspondence: Kim Raines, DNP, RN, CRNP, AGACNP-BC, CCRN, Penn State Erie, The Behrend College, 4701 College Drive, Erie, PA 16563 ([email protected]). Accepted for publication: November 1, 2018 Published ahead of print: December 21, 2018 DOI: 10.1097/NCQ.0000000000000379 318 www.jncqjournal.com J Nurs Care Qual • Vol. 34, No. 4, pp. 318–324 • Copyright © 2018 Wolters Kluwer Health, Inc. All rights reserved. Copyright © 2018 Wolters Kluwer Health, Inc. Unauthorized reproduction of this article is prohibited.

October–December 2019 • Volume 34 • Number 4 www.jncqjournal.com 319 Patients with sepsis transferring directly from the assigned for each element, and scores of 2 or emergency department to the ICU experienced higher constitute a positive qSOFA score. Use mortality of 26%, whereas patients admitted to of qSOFA criteria had a strong predictive value inpatient units and later transferred to the ICU for identifying patients at high risk for poor with sepsis experienced mortality of 40%.6 This outcomes.5 highlights the importance of education for non- ICU nurses that includes the latest sepsis defi- A multidisciplinary sepsis team comprising nitions and strategies for early recognition and physicians, APPs, nurses, and pharmacists at timely, guideline-driven management. our hospital meets regularly to review data on sepsis patients and to evaluate compliance The Centers for Medicare & Medicaid Ser- with national guidelines and CMS benchmarks. vices (CMS) implemented performance bench- Overall, our monthly compliance with CMS marks to guide evidence-based sepsis manage- measures averaged about 50% for a 6-month ment. These are time-sensitive indicators that at period, prompting discussion. One concern was a minimum mandate obtaining blood cultures, that patients may be arriving to the ICU late in administering antibiotics and fluid boluses, and the sepsis continuum. Another concern was that measuring lactate.7 The CMS sepsis QI initia- nurses and providers were unfamiliar with the tives require organizations to demonstrate com- new sepsis definitions and screening tools. pliance with all of the established benchmarks to be eligible for reimbursement. The purpose of this project was to implement a widespread multidisciplinary sepsis education The traditional definition of sepsis cur- initiative for nurses, physicians, and APPs work- rently used by CMS is listed in Supplemen- ing with medical-surgical patients or respond- tal Digital Content Table 1, available at: ing to RRT calls. We hypothesized that targeting http://links.lww.com/JNCQ/A518, and is based sepsis recognition using both qSOFA and or- on systemic inflammatory response criteria, gan dysfunction criteria and empowering nurses an identified source of infection, and evidence to trigger an RRT call based on those criteria of at least 1 organ dysfunction.7 A new def- would significantly impact time-to-sepsis recog- inition of sepsis (Sepsis-3) was introduced in nition while bringing needed resources to the 2016, highlighting mortality risk by assigning bedside for non-ICU patients. The premise was an organ dysfunction score to each of 6 organ that improving time to recognition would sub- systems (Sequential [Sepsis-related] Organ Fail- sequently shorten time to sepsis intervention for ure Assessment [SOFA] score).5 The new sepsis high-risk patients. definition is as follows: “life-threatening organ dysfunction caused by a dysregulated host re- METHODS sponse to infection.”5 Patients with infection and evidence of organ dysfunction (higher Setting and design SOFA scores) had higher mortality than patients This QI project was conducted at a 446-bed with systemic inflammatory response alone.5 tertiary care, level II trauma center. Approval A change in the SOFA score of 2 or more is was obtained from the hospital institutional re- consistent with acute organ dysfunction and view board as a quality initiative. A sepsis ed- is associated with a mortality risk of 10% in ucation program was developed and delivered hospitalized patients with presumed infection.5 to providers including nurses, hospitalists, and APPs for all medical-surgical inpatient areas and While the SOFA organ dysfunction score is ICUs. To evaluate its impact, we conducted a recommended for use in critically ill patients, the pre- and posteducation retrospective descriptive 2016 definitions also introduced use of a sim- evaluation of adult patients, 18 years of age and plified assessment tool for non-ICU patients.5 older, who met CMS criteria for the diagnosis of The quick SOFA (qSOFA) criteria are recom- severe sepsis after transfer from the inpatient unit mended to assess non-ICU patients at risk for to an ICU (either as a result of RRT activation or clinical deterioration.5 The qSOFA score con- independent decision to transfer). We excluded sists of only 3 elements that are easily evaluated from evaluation patients admitted directly from at the bedside: systolic blood pressure, respira- the emergency department to the ICU or from tory rate, and level of consciousness (see Sup- an outlying facility to the ICU and patients who plemental Digital Content Table 1, available at: transitioned to comfort measures within 3 hours http://links.lww.com/JNCQ/A518). One point is of meeting CMS sepsis criteria. Copyright © 2018 Wolters Kluwer Health, Inc. Unauthorized reproduction of this article is prohibited.

320 Sepsis Education Initiative Targeting qSOFA Screening Journal of Nursing Care Quality Patients meeting criteria for severe sepsis were Education was delivered by 2 sepsis education identified from the hospital’s preexisting sepsis nurses who rounded on each unit and conducted database. Electronic records were then reviewed short (average 10 minutes) educational sessions. to identify 30 eligible patients for each of the co- Each nurse received a badge card that attached to horts. For the preimplementation cohort (March his or her identification badge that summarized 2016 through March 2017), the project leader organ dysfunction criteria and the established reviewed 192 patient records to identify 30 pa- hospital criteria for initiating a rapid response tients meeting criteria for inclusion. Following call, and this served as an ongoing reference fol- sepsis education, for the postimplementation co- lowing the education. The card also illustrated hort (May 2017 through December 2017), 181 qSOFA criteria and a treatment prompt labeled records were reviewed to identify 30 patients “5 things in 5 minutes,” which summarized meeting inclusion criteria. the targeted treatments to be accomplished for patients with potential sepsis. Education was Sepsis education initiative delivered on 12 hospital units, and 1000 badge The sepsis education program was developed for cards were distributed to the participants. the hospital by the primary author and deliv- ered to all providers by 2 nurses, increasing the Interprofessional communication was also consistency and fidelity of the intervention. This highlighted in the education. Nurses were in- program targeted (1) early recognition of sepsis structed to specifically include terms that would and use of qSOFA screening for risk assessment, trigger concern for sepsis and sepsis response (2) the importance of initiating prompt, time- when communicating changes in patient con- sensitive treatments, (3) introduction to CMS dition to physicians and APPs, for example, sepsis performance benchmarks, (4) introduc- including phrases such as “My patient meets tion to the new sepsis-3 definitions and goals qSOFA criteria,” or “I am concerned about sep- of treatment, and (5) use of the existing elec- sis.” Nurses were empowered to independently tronic order set for sepsis treatment. The elec- activate RRT calls if qSOFA screening was pos- tronic order set is prepopulated and prompts the itive with a score of 2 or more out of a pos- provider to order evidence-based, time-sensitive sible 3 or to notify the physician or the APP diagnostic studies and sepsis interventions. Use of these changes in condition. Hospitalists and of the electronic order set is encouraged to facili- APPs were prompted to respond to these calls tate compliance with the timing of blood cultures with urgency. Nurses were instructed that hand- and sequential lactates (laboratory responds to off communication between inpatient units and all RRT calls), timely completion of fluid bo- ICU should include the concern for sepsis and re- luses, and effective communication of antibiotic port on the initiation of diagnostic tests and tim- urgency to the pharmacy. When fluids and an- ing of treatments to facilitate completion of fluid tibiotics are ordered using the electronic order boluses and administration of antibiotics espe- set, the order is then flagged for pharmacy as ur- cially if not accomplished prior to transfer. This gent because of suspected sepsis and prioritized strategy was designed to ensure seamless care for to prompt immediate action. Orders placed out- the patients, regardless of locale. Once the sepsis side of the order set do not necessarily trigger the education was completed, qSOFA screening was same urgent response in the pharmacy queue. implemented hospital-wide for nurses to use as a common mechanism to prompt early identifica- All physicians and APPs on the hospitalist tion of sepsis, initiation of an RRT call, and esca- team, RRT members (nurses, ICU charge nurses, lation of care (as needed) in collaboration with ICU physicians, and APPs), and nurses from RRT responders. each inpatient unit and ICU participated in the educational initiative. Staff from the emergency Outcome measures department, postanesthesia care unit, and outpa- tient and procedural units were excluded. Edu- Sepsis recognition and RRT time cation was accomplished during April and May Sepsis recognition was recorded by the project 2017, with a combination of lectures, slide pre- leader via review of electronic records to deter- sentations, and supplemental teaching materials. mine the time at which each patient met cri- Staff were educated either formally at staff meet- teria for sepsis by the traditional CMS sepsis ings or via informal presentations on each unit. definition and met qSOFA criteria to determine whether patients at risk were identified earlier by Copyright © 2018 Wolters Kluwer Health, Inc. Unauthorized reproduction of this article is prohibited.

October–December 2019 • Volume 34 • Number 4 www.jncqjournal.com 321 use of the qSOFA screening. The triggers for pos- t test (age) or the nonparametric Mann-Whitney itive qSOFA scores were recorded as well as the U test. indication for initiating an RRT call (respiratory, neurologic, or hypotension). The timing of the RESULTS RRT call in relation to hospital admission was There were no significant differences between the recorded. pre- and postimplementation groups in age, gen- der, comorbidities, or discharge disposition (see Time to treatment for sepsis interventions Supplemental Digital Content Table 2, available We evaluated the time intervals between RRT at: http://links.lww.com/JNCQ/A519). Seven pa- call and time-sensitive sepsis interventions. If the tients (23%) in the pregroup and 10 patients patient was transferred electively to the ICU and (33%) in the postimplementation group died in not part of an RRT call, the time of ICU transfer the hospital. Median length of stay was signifi- was used in lieu of RRT time. The ICU trans- cantly shorter in the postimplementation group fer time was defined by the first documented by 4.8 days (pre: 13.6, post: 8.8; P = .025). More ICU vital signs. Similarly, we evaluated time from than 80% of patients in both groups had sepsis sepsis recognition by both CMS criteria and identified in clinical notes prior to the RRT call. qSOFA criteria to each sepsis intervention. The time-sensitive sepsis interventions included time Sepsis recognition and RRT call to blood cultures, antibiotic administration, first After the sepsis education initiative, there was a lactate measurement, and completion of fluid bo- statistically significant improvement in median lus of 30 mL/kg, all reported in hours. time to RRT for patients meeting qSOFA crite- ria from 11.8 hours pre [interquartile range: 3.4, Compliance with time-sensitive sepsis 34.3] to 1.7 hours post [interquartile range: 0, interventions 11.7], P = .005 (Table). The timing of the RRT in We noted the percentages of patients in each relation to admission did not differ significantly group meeting each of the time-sensitive sepsis between groups, but there were differences in the interventions from the time of sepsis identifica- physiologic trigger for the RRT call with signif- tion by both CMS criteria and qSOFA criteria. icantly more patients with a respiratory event in the preimplementation group (83% vs 37% post, Data collection P < .001) and significantly more hypotension as The project leader screened electronic records for trigger in the postimplementation group (13% eligibility and then collected data from each of pre vs 50% post, P = .002). the 60 patients, recording (1) demographics and comorbidities, length of stay, and discharge dis- Time to treatment for sepsis interventions position; (2) the time at which each patient met Time to each sepsis intervention was recorded criteria for sepsis by CMS sepsis definition and from RRT call and from the time of sepsis iden- qSOFA criteria; (3) the time of RRT call and tification by both CMS criteria and qSOFA crite- physiologic triggers for the RRT call; and (4) the ria (Table). In both groups, blood cultures were times from RRT call and identification of sepsis drawn before the RRT call, and there were no to each treatment intervention (blood cultures, significant differences between groups in time to antibiotics, initial lactate, and fluid bolus). blood cultures. A significant reduction in time from qSOFA criteria to time of antibiotic admin- Data analysis istration was noted between the pre- and postim- Data were analyzed using IBM SPSS statistics plementation groups (1.4 [−2.4, 6.2] hours pre version 24 (Armonk, New York). Categorical vs −4.7 [−25.4, 1.8] hours [prior to meeting data were reported as frequency and percent- qSOFA criteria] post, P = .009) (Table). Time age within group, and between-group compar- to fluid bolus administration from RRT call isons were done using either χ 2 test or Fisher improved for both CMS and qSOFA groups, exact test. Continuous data were reported as though it did not reach statistical significance for mean with standard deviation (age) or median either group (Table). with interquartile range, and comparisons be- tween groups were done using either the Student Copyright © 2018 Wolters Kluwer Health, Inc. Unauthorized reproduction of this article is prohibited.

322 Sepsis Education Initiative Targeting qSOFA Screening Journal of Nursing Care Quality Table. Outcomes: Sepsis Recognition, Treatments, and Compliance With Time-Sensitive Sepsis Interventions Variable Pre, N = 30 Post, N = 30 P Sepsis recognition: time to RRT, h Median (IQR) Median (IQR) .569 CMS criteria to RRT 11.1 (3.2, 26.7) 7.4 (3.3, 43.2) .005 qSOFA criteria to RRT 11.8 (3.4, 34.3) 1.7 (0, 11.7) Sepsis treatments: time to intervention, ha Blood cultures − 7.4 (−29.3, −0.5) − 4.4 (−13.9, 0.7) .352 0.0 (−1.0, 9.6) 0.0 (0.0, 4.5) .766 RRT to blood cultures 0.2 (−2.5, 16.6) .176 CMS to blood cultures − 1.4 (−8.9, 4.9) qSOFA to blood cultures − 11.9 (−61.7, −2.8) .871 Antibiotics 1.7 (−0.3, 5.5) − 7.6 (−66.2, −2.4) .139 RRT to antibiotics 1.4 (−2.4, 6.2) 0.7 (−2.0, 2.7) .009 CMS to antibiotics N = 20 qSOFA to antibiotics 2.3 (−16.5, 8.7) − 4.7 (−25.4, 1.8) .679 Fluid bolus of 30 mL/kg 6.8 (0.1, 24.5) N = 23 .846 RRT to fluid bolus 6.0 (2.0, 24.2) .137 CMS to fluid bolus N (%) − 1.1 (−4.8, 11.6) qSOFA to fluid bolus 6.3 (1.7, 14.2) 19 (63) 2.3 (−4.7, 15.5) Patient compliance with sepsis interventions 17 (57) N (%) Blood cultures within 1 h (or 24 h prior) CMS criteria 20 (67) 17 (57) .598 qSOFA criteria 18 (60) 16 (53) .795 Antibiotics within 3 h (or started prior) 11 (37) 25 (83) .136 CMS criteria 8 (27) 26 (87) .02 qSOFA criteria 13 (43) 16 (53) .194 Lactate within 3 h pre or post 12 (40) 8 (27) .999 CMS criteria qSOFA criteria 8 (27) .176 15 (50) .436 Fluid bolus of 30 mL/kg within 3 h CMS criteria qSOFA criteria Abbreviations: CMS, Centers for Medicare & Medicaid Services; IQR, interquartile range; qSOFA, quick Sequential Organ Failure Assessment; RRT, rapid response team call. aA negative number means that intervention occurred prior to RRT call or sepsis identification. Values in boldface indicate significant P value. Compliance with time-sensitive sepsis sepsis identification (either by CMS criteria or by qSOFA criteria), with all groups above 50% interventions compliance. Compliance with antibiotic admin- The percentages of patients in compliance with istration within 3 hours of sepsis identification each of the time-sensitive treatments are noted improved significantly in the qSOFA group from in the Table. The definitions for assessing com- 60% of patients in the preimplementation group pliance are listed in Supplemental Digital Con- to 87% of patients in the postimplementation tent Table 1, available at: http://links.lww.com/ group, P = .02. Compliance with completing JNCQ/A518. There were no significant differ- the 30 mL/kg fluid bolus remained at less than ences between groups in the proportion of pa- 50% of patients in each group both pre and tients having blood cultures within 1 hour of Copyright © 2018 Wolters Kluwer Health, Inc. Unauthorized reproduction of this article is prohibited.

October–December 2019 • Volume 34 • Number 4 www.jncqjournal.com 323 postimplementation. Of note, the CMS criteria They propose the use of automated electronic can be met without hypotension, and compliance health record data surveillance applying Mod- with fluid bolus required a full 30 mL/kg bolus. ified Early Warning Signs-Sepsis Recognition Compliance with first lactate measure remained Score (MEWS-SRS) that showed promising im- low in both groups as well. pact on early intervention.10 We had a compa- rable improvement in sepsis recognition when DISCUSSION teaching nurses to use qSOFA to activate RRT The high number of patients with a diagnosis calls (the postimplementation group decreased of sepsis prior to the RRT (87% pre and 83% their RRT activation time almost by 9 hours post) is an important finding as it reinforces the in our small sample). The negative aspect re- need for providing sepsis education to non-ICU lated to electronic tools includes alarm fatigue nurses to promote early identification and early and cost of implementation. Our objective was treatment of these high-risk patients. Educating to cost-effectively impact recognition on septic on qSOFA and empowering nurses to call RRT patients with the resources available at our hos- based on qSOFA-positive scores were associated pital. Implementation of electronic warning sys- with shorter time to RRT and possibly shortened tems comes with higher cost. We acknowledge the time to intervention after the sepsis education the limitation of an education-only intervention initiative. with potential wear off effect and the need for ongoing education to sustain improvement.11 As A recent retrospective Australian study by part of this initiative, we are planning to add LeGuen et al8 conducted in a large tertiary hospi- this education to the mandatory yearly education tal found that nearly 40% of RRT patients were package for nurses. Our QI was limited to 1 in- qSOFA positive and subsequently had a signif- tervention, education. Other strategies suggested icant difference in rates to ICU admission, re- by Yost et al11 such as reminders, feedbacks, and peat RRT, and inhospital death compared with audits could be completed and provide leverage infected patients who were qSOFA negative. This for our results to increase the impact of our inter- study reinforces the relevance of evaluating pa- vention in the long term. As part of a continuing tients with qSOFA-positive scores. LeGuen et al8 QI initiative, these interventions will be consid- limited their evaluation to validating qSOFA ered for future application. after RRT was called whereas our education fo- cus was to use qSOFA as the activation criteria Limitations for RRT calls. Our results suggest that using The sample size in each group is small, limiting qSOFA to trigger an RRT call is a valid approach the strength of some associations and the abil- to get help to the bedside and to initiate prompt ity to generalize results. This study is not pow- intervention (blood cultures, lactate measures, ered to evaluate mortality outcomes but it is to antibiotic use, and fluid bolus) for sepsis pa- serve as proof of concept for future efforts on tients in the medical ward at high risk for poor QI. This project was conducted at a single ter- outcomes. tiary level II trauma center, which may limit gen- eralizability. Data were collected retrospectively, Delmas et al9 documented that a sepsis team relying on existing documentation that may have performed superiorly with regard to intervention limited the ability to specifically time the identi- led by qSOFA in a retrospective analysis of about fication of sepsis. 1000 patients in a tertiary medical center. This reinforces our premise that qSOFA can be use- CONCLUSIONS ful to lead early sepsis recognition. Our initiative A hospital-wide multidisciplinary sepsis educa- differs from Delmas et al because in our hospital, tion program targeting sepsis recognition using the RRT team is in charge of responding to all both qSOFA and organ dysfunction criteria em- inward emergencies, and we do not have a dedi- powered nurses to trigger an RRT call based on cated sepsis team. However, both results suggest those criteria. Subsequently, time-to-sepsis recog- an improvement in bundle compliance, which nition and RRT activation for patients meeting has been the expectation by CMS and other reg- qSOFA criteria resulted in a shortened time to ulatory agencies.6 some sepsis interventions, most notably antibi- otic administration. This nurse-driven education A different approach to early recognition for sepsis in the medicine ward is electronic snif- fers such as the one reported by Guirgis et al.10 Copyright © 2018 Wolters Kluwer Health, Inc. Unauthorized reproduction of this article is prohibited.

324 Sepsis Education Initiative Targeting qSOFA Screening Journal of Nursing Care Quality initiative provided an evidence-based platform international consensus definitions for sepsis and septic for enhanced communication between disci- shock (sepsis-3). JAMA. 2016;315(8):801-810. plines, facilitating faster, criteria-based evalua- 6. Schorr C, Odden A, Evans L, et al. Implementation of a mul- tion of patients by a multidisciplinary team. ticenter performance improvement program for early de- Patient-centered interventions (timing of RRT tection and treatment of severe sepsis in general medical- call and time to antibiotics) served as the mea- surgical wards. J Hosp Med. 2016;11(suppl 1):S32-S39. sures of success for this project. 7. Santistevan M. American College of Emergency Physi- cians Quality Improvement Patient Safety Section. Sepsis REFERENCES CMS core measure (Sep-1) highlights. https://www.acep. org/how-we-serve/sections/quality-improvement–patient- 1. Angus DC, Linde-Zwirble WT, Lidicker J, Clermont G, Car- safety/newsletters/march-2016/sepsis-cms-core-measure- cillo J, Pinsky MR. Epidemiology of severe sepsis in the sep-1-highlights/#sm.000013cc045ccafrjphfifr1scrqb. United States: analysis of incidence, outcome, and associated Published March 2016. Accessed September 20, 2016. costs of care. Crit Care Med. 2001;29(7):1303-1310. 8. LeGuen M, Ballueer Y, McKay R, et al. Frequency and significance of qSOFA criteria during adult rapid response 2. Stoller J, Halpin L, Weis M, et al. Epidemiology of severe team reviews: a prospective cohort study. Resuscitation. sepsis: 2008-2012. J Crit Care. 2016;31(1):58-62. 2018;122:13-18. 9. Delmas T, Price J, Birdwell A, et al. Impact of a sepsis team 3. Cross G, Bilgrami I, Eastwood GM, et al. The epidemiology on outcomes in patients with sepsis on the wards. Chest. of sepsis during rapid response team reviews in a teaching 2017;152(4 suppl):A400. hospital. Anaesth Intensive Care. 2015;43(2):193-198 10. Guirgis FW, Jones L, Esma R, et al. Managing sepsis: elec- tronic recognition, rapid response teams, and standardized 4. Barwise AT, Thongprayoon C, Gajic O, Jensen J, Herasevich care save lives. J Crit Care. 2017;40:296-302. V, Pickering BW. Delayed rapid response team activation is 11. Yost J, Ganann R, Thompson D, et al. The effective- associated with increased hospital mortality, morbidity, and ness of knowledge translation interventions for promot- length of stay in a tertiary care institution. Crit Care Med. ing evidence-informed decision-making among nurses in ter- 2016;44(1):54-63. tiary care: a systematic review and meta-analysis. Implement Sci. 2015;10(1):98. 5. Singer M, Deutschman M, Seymour CW, et al. The third Copyright © 2018 Wolters Kluwer Health, Inc. Unauthorized reproduction of this article is prohibited.