Semin Respir Crit Care Med 2021; 42(05): 706-716
DOI: 10.1055/s-0041-1733899
Review Article

Evidence for the Application of Sepsis Bundles in 2021

Erika P. Plata-Menchaca
1   Shock, Organ Dysfunction and Resuscitation Research Group, Vall d'Hebron Institut de Recerca (VHIR), Vall d'Hebron Hospital Universitari, Barcelona, Spain
2   Department of Intensive Care, Hospital Clínic de Barcelona, Barcelona, Spain
,
Juan Carlos Ruiz-Rodríguez
1   Shock, Organ Dysfunction and Resuscitation Research Group, Vall d'Hebron Institut de Recerca (VHIR), Vall d'Hebron Hospital Universitari, Barcelona, Spain
3   Department of Intensive Care, Vall d'Hebron Hospital Universitari, Vall d'Hebron, Barcelona, Spain
4   Department of Medicine, Universitat Autonoma de Barcelona, Bellaterra, Barcelona, Spain
,
Ricard Ferrer
1   Shock, Organ Dysfunction and Resuscitation Research Group, Vall d'Hebron Institut de Recerca (VHIR), Vall d'Hebron Hospital Universitari, Barcelona, Spain
3   Department of Intensive Care, Vall d'Hebron Hospital Universitari, Vall d'Hebron, Barcelona, Spain
4   Department of Medicine, Universitat Autonoma de Barcelona, Bellaterra, Barcelona, Spain
› Author Affiliations

Abstract

Sepsis represents a severe condition that predisposes patients to a high risk of death if its progression is not ended. As with other time-dependent conditions, the performance of determinant interventions has led to significant survival benefits and quality-of-care improvements in acute emergency care. Thus, the initial interventions in sepsis are a cornerstone for prognosis in most patients. Even though the evidence supporting the hour-1 bundle is perfectible, real-life application of thoughtful and organized sepsis care has improved survival and quality of care in settings promoting compliance to evidence-based treatments. Current evidence for implementing the Surviving Sepsis Campaign bundles for early sepsis management is moving forward to better approaches as more substantial evidence evolves.



Publication History

Article published online:
20 September 2021

© 2021. Thieme. All rights reserved.

Thieme Medical Publishers, Inc.
333 Seventh Avenue, 18th Floor, New York, NY 10001, USA

 
  • References

  • 1 Prescott HC, Angus DC. Enhancing recovery from sepsis: a review. JAMA 2018; 319 (01) 62-75
  • 2 Rhodes A, Evans LE, Alhazzani W. et al. Surviving sepsis campaign: international guidelines for management of sepsis and septic shock: 2016. Intensive Care Med 2017; 43 (03) 304-377
  • 3 Burns PB, Rohrich RJ, Chung KC. The levels of evidence and their role in evidence-based medicine. Plast Reconstr Surg 2011; 128 (01) 305-310
  • 4 Jones DS, Grady C, Lederer SE. “Ethics and Clinical Research” – the 50th anniversary of Beecher's bombshell. N Engl J Med 2016; 374 (24) 2393-2398
  • 5 Nardini C. The ethics of clinical trials. Ecancermedicalscience 2014; 8: 387
  • 6 Prescott HC, Cope TM, Gesten FC. et al. Reporting of sepsis cases for performance measurement versus for reimbursement in New York State. Crit Care Med 2018; 46 (05) 666-673
  • 7 Levy MM, Evans LE, Rhodes A. The surviving Sepsis Campaign Bundle: 2018 update. Intensive Care Med 2018; 44 (06) 925-928
  • 8 Seymour CW, Gesten F, Prescott HC. et al. Time to treatment and mortality during mandated emergency care for sepsis. N Engl J Med 2017; 376 (23) 2235-2244
  • 9 Miller III RR, Dong L, Nelson NC. et al; Intermountain Healthcare Intensive Medicine Clinical Program. Multicenter implementation of a severe sepsis and septic shock treatment bundle. Am J Respir Crit Care Med 2013; 188 (01) 77-82
  • 10 Ferrer R, Martínez ML, Gomà G. et al; ABISS-Edusepsis Study Group. Improved empirical antibiotic treatment of sepsis after an educational intervention: the ABISS-Edusepsis study. Crit Care 2018; 22 (01) 167
  • 11 Ferrer R, Artigas A, Suarez D. et al; Edusepsis Study Group. Effectiveness of treatments for severe sepsis: a prospective, multicenter, observational study. Am J Respir Crit Care Med 2009; 180 (09) 861-866
  • 12 Esteban E, Belda S, García-Soler P. et al. A multifaceted educational intervention shortened time to antibiotic administration in children with severe sepsis and septic shock: ABISS Edusepsis pediatric study. Intensive Care Med 2017; 43 (12) 1916-1918
  • 13 https://www.cms.gov/Newsroom/MediaReleaseDatabase/Fact-sheets/2014-Fact-sheets-items/2014-08-04-2.html . Accessed July 10, 2021
  • 14 Giuliano KK, Lecardo M, Staul L. Impact of protocol watch on compliance with the Surviving Sepsis Campaign. Am J Crit Care 2011; 20 (04) 313-321
  • 15 Coba V, Whitmill M, Mooney R. et al; The Henry Ford Hospital Sepsis Collaborative Group. Resuscitation bundle compliance in severe sepsis and septic shock: improves survival, is better late than never. J Intensive Care Med 2011; 26 (05) 304-313
  • 16 Barochia AV, Cui X, Vitberg D. et al. Bundled care for septic shock: an analysis of clinical trials. Crit Care Med 2010; 38 (02) 668-678
  • 17 Pruinelli L, Westra BL, Yadav P. et al. Delay within the 3-hour surviving sepsis campaign guideline on mortality for patients with severe sepsis and septic shock. Crit Care Med 2018; 46 (04) 500-505
  • 18 Baghdadi JD, Brook RH, Uslan DZ. et al. Association of a care bundle for early sepsis management with mortality among patients with hospital-onset or community-onset sepsis. JAMA Intern Med 2020; 180 (05) 707-716
  • 19 Kahn JM, Davis BS, Yabes JG. et al. Association between state-mandated protocolized sepsis care and in-hospital mortality among adults with sepsis. JAMA 2019; 322 (03) 240-250
  • 20 Levy MM, Gesten FC, Phillips GS. et al; The Results of the New York State Initiative. Mortality changes associated with mandated public reporting for sepsis. Am J Respir Crit Care Med 2018; 198 (11) 1406-1412
  • 21 Evans IVR, Phillips GS, Alpern ER. et al. Association between the New York sepsis care mandate and in-hospital mortality for pediatric sepsis. JAMA 2018; 320 (04) 358-367
  • 22 Bourne DS, Davis BS, Gigli KH. et al. Economic analysis of mandated protocolized sepsis care in New York hospitals. Crit Care Med 2020; 48 (10) 1411-1418
  • 23 Husabø G, Nilsen RM, Flaatten H. et al. Early diagnosis of sepsis in emergency departments, time to treatment, and association with mortality: an observational study. PLoS One 2020; 15 (01) e0227652
  • 24 Laupland KB, Ferrer R. Is it time to implement door-to-needle time for “infection attacks”?. Intensive Care Med 2017; 43 (11) 1712-1713
  • 25 García-de-Acilu M, Mesquida J, Gruartmoner G, Ferrer R. Hemodynamic support in septic shock. Curr Opin Anaesthesiol 2021; 34 (02) 99-106
  • 26 Lat I, Coopersmith CM, De Backer D, Coopersmith CM. Research Committee of the Surviving Sepsis Campaign. The surviving sepsis campaign: fluid resuscitation and vasopressor therapy research priorities in adult patients. Intensive Care Med Exp 2021; 9 (01) 10
  • 27 Funk DJ, Jacobsohn E, Kumar A. The role of venous return in critical illness and shock-part I: physiology. Crit Care Med 2013; 41 (01) 255-262
  • 28 Funk DJ, Jacobsohn E, Kumar A. Role of the venous return in critical illness and shock: part II-shock and mechanical ventilation. Crit Care Med 2013; 41 (02) 573-579
  • 29 Malbrain MLNG, Van Regenmortel N, Saugel B. et al. Principles of fluid management and stewardship in septic shock: it is time to consider the four D's and the four phases of fluid therapy. Ann Intensive Care 2018; 8 (01) 66
  • 30 Hoste EA, Maitland K, Brudney CS. et al; ADQI XII Investigators Group. Four phases of intravenous fluid therapy: a conceptual model. Br J Anaesth 2014; 113 (05) 740-747
  • 31 Finfer S, Bellomo R, Boyce N, French J, Myburgh J, Norton R. SAFE Study Investigators. A comparison of albumin and saline for fluid resuscitation in the intensive care unit. N Engl J Med 2004; 350 (22) 2247-2256
  • 32 Angus DC. Early, goal-directed therapy for septic shock - a patient-level meta-analysis. N Engl J Med 2017; 377 (10) 995
  • 33 Maitland K, Kiguli S, Opoka RO. et al; FEAST Trial Group. Mortality after fluid bolus in African children with severe infection. N Engl J Med 2011; 364 (26) 2483-2495
  • 34 Andrews B, Muchemwa L, Kelly P, Lakhi S, Heimburger DC, Bernard GR. Simplified severe sepsis protocol: a randomized controlled trial of modified early goal-directed therapy in Zambia. Crit Care Med 2014; 42 (11) 2315-2324
  • 35 Andrews B, Semler MW, Muchemwa L. et al. Effect of an early resuscitation protocol on in-hospital mortality among adults with sepsis and hypotension: a randomized clinical trial. JAMA 2017; 318 (13) 1233-1240
  • 36 Dellinger RP, Schorr CA, Levy MM. A users' guide to the 2016 Surviving Sepsis Guidelines. Intensive Care Med 2017; 43 (03) 299-303
  • 37 Buchman TG, Azoulay E. Practice guidelines as implementation science: the journal editors' perspective. Intensive Care Med 2017; 43 (03) 378-379
  • 38 Vincent JL, De Backer D. Circulatory shock. N Engl J Med 2013; 369 (18) 1726-1734
  • 39 Self WH, Semler MW, Bellomo R. et al; CLOVERS Protocol Committee and NHLBI Prevention and Early Treatment of Acute Lung Injury (PETAL) Network Investigators. Liberal versus restrictive intravenous fluid therapy for early septic shock: rationale for a randomized trial. Ann Emerg Med 2018; 72 (04) 457-466
  • 40 Hjortrup PB, Haase N, Bundgaard H. et al; CLASSIC Trial Group, Scandinavian Critical Care Trials Group. Restricting volumes of resuscitation fluid in adults with septic shock after initial management: the CLASSIC randomised, parallel-group, multicentre feasibility trial. Intensive Care Med 2016; 42 (11) 1695-1705
  • 41 Cecconi M, Hofer C, Teboul JL. et al; FENICE Investigators, ESICM Trial Group. Fluid challenges in intensive care: the FENICE study: a global inception cohort study. Intensive Care Med 2015; 41 (09) 1529-1537
  • 42 Sakr Y, Rubatto Birri PN, Kotfis K. et al; Intensive Care Over Nations Investigators. Higher fluid balance increases the risk of death from sepsis: results from a large international audit. Crit Care Med 2017; 45 (03) 386-394
  • 43 Milford EM, Reade MC. Resuscitation fluid choices to preserve the endothelial glycocalyx. Crit Care 2019; 23 (01) 77
  • 44 Sennoun N, Montemont C, Gibot S, Lacolley P, Levy B. Comparative effects of early versus delayed use of norepinephrine in resuscitated endotoxic shock. Crit Care Med 2007; 35 (07) 1736-1740
  • 45 Avni T, Lador A, Lev S, Leibovici L, Paul M, Grossman A. Vasopressors for the treatment of septic shock: systematic review and meta-analysis. PLoS One 2015; 10 (08) e0129305
  • 46 De Backer D, Biston P, Devriendt J. et al; SOAP II Investigators. Comparison of dopamine and norepinephrine in the treatment of shock. N Engl J Med 2010; 362 (09) 779-789
  • 47 Levy B. Bench-to-bedside review: Is there a place for epinephrine in septic shock?. Crit Care 2005; 9 (06) 561-565
  • 48 Gordon AC, Mason AJ, Thirunavukkarasu N. et al; VANISH Investigators. Effect of early vasopressin vs norepinephrine on kidney failure in patients with septic shock: the VANISH randomized clinical trial. JAMA 2016; 316 (05) 509-518
  • 49 Tumlin JA, Murugan R, Deane AM. et al; Angiotensin II for the Treatment of High-Output Shock 3 (ATHOS-3) Investigators. Outcomes in patients with vasodilatory shock and renal replacement therapy treated with intravenous angiotensin II. Crit Care Med 2018; 46 (06) 949-957
  • 50 Wu JY, Stollings JL, Wheeler AP, Semler MW, Rice TW. Efficacy and outcomes after vasopressin guideline implementation in septic shock. Ann Pharmacother 2017; 51 (01) 13-20
  • 51 Asfar P, Meziani F, Hamel JF. et al; SEPSISPAM Investigators. High versus low blood-pressure target in patients with septic shock. N Engl J Med 2014; 370 (17) 1583-1593
  • 52 Lamontagne F, Richards-Belle A, Thomas K. et al; 65 Trial Investigators. Effect of reduced exposure to vasopressors on 90-day mortality in older critically ill patients with vasodilatory hypotension: a randomized clinical trial. JAMA 2020; 323 (10) 938-949
  • 53 Lamontagne F, Day AG, Meade MO. et al. Pooled analysis of higher versus lower blood pressure targets for vasopressor therapy septic and vasodilatory shock. Intensive Care Med 2018; 44 (01) 12-21
  • 54 Jones AE, Shapiro NI, Trzeciak S, Arnold RC, Claremont HA, Kline JA. Emergency Medicine Shock Research Network (EMShockNet) Investigators. Lactate clearance vs central venous oxygen saturation as goals of early sepsis therapy: a randomized clinical trial. JAMA 2010; 303 (08) 739-746
  • 55 Jansen TC, van Bommel J, Schoonderbeek FJ. et al; LACTATE Study Group. Early lactate-guided therapy in intensive care unit patients: a multicenter, open-label, randomized controlled trial. Am J Respir Crit Care Med 2010; 182 (06) 752-761
  • 56 Peake SL, Delaney A, Bailey M. et al; ARISE Investigators, ANZICS Clinical Trials Group. Goal-directed resuscitation for patients with early septic shock. N Engl J Med 2014; 371 (16) 1496-1506
  • 57 Mouncey PR, Osborn TM, Power GS. et al; ProMISe Trial Investigators. Trial of early, goal-directed resuscitation for septic shock. N Engl J Med 2015; 372 (14) 1301-1311
  • 58 Yealy DM, Kellum JA, Huang DT. et al; ProCESS Investigators. A randomized trial of protocol-based care for early septic shock. N Engl J Med 2014; 370 (18) 1683-1693
  • 59 Shapiro NI, Howell MD, Talmor D. et al. Serum lactate as a predictor of mortality in emergency department patients with infection. Ann Emerg Med 2005; 45 (05) 524-528
  • 60 Mikkelsen ME, Miltiades AN, Gaieski DF. et al. Serum lactate is associated with mortality in severe sepsis independent of organ failure and shock. Crit Care Med 2009; 37 (05) 1670-1677
  • 61 Bhat SR, Swenson KE, Francis MW, Wira CR. Lactate clearance predicts survival among patients in the emergency department with severe sepsis. West J Emerg Med 2015; 16 (07) 1118-1126
  • 62 Casserly B, Phillips GS, Schorr C. et al. Lactate measurements in sepsis-induced tissue hypoperfusion: results from the Surviving Sepsis Campaign database. Crit Care Med 2015; 43 (03) 567-573
  • 63 Lee SG, Song J, Park DW. et al. Prognostic value of lactate levels and lactate clearance in sepsis and septic shock with initial hyperlactatemia: a retrospective cohort study according to the Sepsis-3 definitions. Medicine (Baltimore) 2021; 100 (07) e24835
  • 64 Lyu X, Xu Q, Cai G, Yan J, Yan M. [Efficacies of fluid resuscitation as guided by lactate clearance rate and central venous oxygen saturation in patients with septic shock]. Zhonghua Yi Xue Za Zhi 2015; 95 (07) 496-500
  • 65 Gu WJ, Zhang Z, Bakker J. Early lactate clearance-guided therapy in patients with sepsis: a meta-analysis with trial sequential analysis of randomized controlled trials. Intensive Care Med 2015; 41 (10) 1862-1863
  • 66 Simpson SQ, Gaines M, Hussein Y, Badgett RG. Early goal-directed therapy for severe sepsis and septic shock: a living systematic review. J Crit Care 2016; 36: 43-48
  • 67 Hernández G, Ospina-Tascón GA, Damiani LP. et al; The ANDROMEDA SHOCK Investigators and the Latin America Intensive Care Network (LIVEN). Effect of a resuscitation strategy targeting peripheral perfusion status vs serum lactate levels on 28-day mortality among patients with septic shock: the ANDROMEDA-SHOCK randomized clinical trial. JAMA 2019; 321 (07) 654-664
  • 68 Plata-Menchaca EP, Ferrer R. Life-support tools for improving performance of the Surviving Sepsis Campaign Hour-1 bundle. Med Intensiva (Engl Ed) 2018; 42 (09) 547-550
  • 69 Kim HI, Park S. Sepsis: early recognition and optimized treatment. Tuberc Respir Dis (Seoul) 2019; 82 (01) 6-14
  • 70 Ramar K, Gajic O. Early recognition and treatment of severe sepsis. Am J Respir Crit Care Med 2013; 188 (01) 7-8
  • 71 Ranieri VM, Thompson BT, Barie PS. et al; PROWESS-SHOCK Study Group. Drotrecogin alfa (activated) in adults with septic shock. N Engl J Med 2012; 366 (22) 2055-2064
  • 72 Levy MM, Rhodes A, Phillips GS. et al. Surviving Sepsis Campaign: association between performance metrics and outcomes in a 7.5-year study. Crit Care Med 2015; 43 (01) 3-12
  • 73 Coz Yataco A, Jaehne AK, Rivers EP. Protocolized early sepsis care is not only helpful for patients: it prevents medical errors. Crit Care Med 2017; 45 (03) 464-472
  • 74 Cassini A, Högberg LD, Plachouras D. et al; Burden of AMR Collaborative Group. Attributable deaths and disability-adjusted life-years caused by infections with antibiotic-resistant bacteria in the EU and the European Economic Area in 2015: a population-level modelling analysis. Lancet Infect Dis 2019; 19 (01) 56-66
  • 75 Gerding DN. The search for good antimicrobial stewardship. Jt Comm J Qual Improv 2001; 27 (08) 403-404
  • 76 Singer M. Antibiotics for sepsis: does each hour really count, or is it incestuous amplification?. Am J Respir Crit Care Med 2017; 196 (07) 800-802
  • 77 Bernhard M, Lichtenstern C, Eckmann C, Weigand MA. The early antibiotic therapy in septic patients–milestone or sticking point?. Crit Care 2014; 18 (06) 671
  • 78 Mi MY, Klompas M, Evans L. Early administration of antibiotics for suspected sepsis. N Engl J Med 2019; 380 (06) 593-596
  • 79 Beumier M, Casu GS, Hites M. et al. Elevated β-lactam concentrations associated with neurological deterioration in ICU septic patients. Minerva Anestesiol 2015; 81 (05) 497-506
  • 80 Garey KW, Rege M, Pai MP. et al. Time to initiation of fluconazole therapy impacts mortality in patients with candidemia: a multi-institutional study. Clin Infect Dis 2006; 43 (01) 25-31
  • 81 Bodey GP, Jadeja L, Elting L. Pseudomonas bacteremia. Retrospective analysis of 410 episodes. Arch Intern Med 1985; 145 (09) 1621-1629
  • 82 Garnacho-Montero J, García-Cabrera E, Diaz-Martín A. et al. Determinants of outcome in patients with bacteraemic pneumococcal pneumonia: importance of early adequate treatment. Scand J Infect Dis 2010; 42 (03) 185-192
  • 83 Gacouin A, Le Tulzo Y, Lavoue S. et al. Severe pneumonia due to Legionella pneumophila: prognostic factors, impact of delayed appropriate antimicrobial therapy. Intensive Care Med 2002; 28 (06) 686-691
  • 84 Hamandi B, Holbrook AM, Humar A. et al. Delay of adequate empiric antibiotic therapy is associated with increased mortality among solid-organ transplant patients. Am J Transplant 2009; 9 (07) 1657-1665
  • 85 Harmankaya M, Oreskov JO, Burcharth J, Gogenur I. The impact of timing of antibiotics on in-hospital outcomes after major emergency abdominal surgery. Eur J Trauma Emerg Surg 2018; 46 (01) 221-227
  • 86 Gaieski DF, Mikkelsen ME, Band RA. et al. Impact of time to antibiotics on survival in patients with severe sepsis or septic shock in whom early goal-directed therapy was initiated in the emergency department. Crit Care Med 2010; 38 (04) 1045-1053
  • 87 Liu VX, Fielding-Singh V, Greene JD. et al. The timing of early antibiotics and hospital mortality in sepsis. Am J Respir Crit Care Med 2017; 196 (07) 856-863
  • 88 Puskarich MA, Trzeciak S, Shapiro NI. et al; Emergency Medicine Shock Research Network (EMSHOCKNET). Association between timing of antibiotic administration and mortality from septic shock in patients treated with a quantitative resuscitation protocol. Crit Care Med 2011; 39 (09) 2066-2071
  • 89 Zhang D, Micek ST, Kollef MH. Time to appropriate antibiotic therapy is an independent determinant of postinfection ICU and hospital lengths of stay in patients with sepsis. Crit Care Med 2015; 43 (10) 2133-2140
  • 90 Bagshaw SM, Lapinsky S, Dial S. et al; Cooperative Antimicrobial Therapy of Septic Shock (CATSS) Database Research Group. Acute kidney injury in septic shock: clinical outcomes and impact of duration of hypotension prior to initiation of antimicrobial therapy. Intensive Care Med 2009; 35 (05) 871-881
  • 91 Iscimen R, Cartin-Ceba R, Yilmaz M. et al. Risk factors for the development of acute lung injury in patients with septic shock: an observational cohort study. Crit Care Med 2008; 36 (05) 1518-1522
  • 92 Garnacho-Montero J, Aldabo-Pallas T, Garnacho-Montero C. et al. Timing of adequate antibiotic therapy is a greater determinant of outcome than are TNF and IL-10 polymorphisms in patients with sepsis. Crit Care 2006; 10 (04) R111
  • 93 Hwang SY, Shin J, Jo IJ. et al. Delayed antibiotic therapy and organ dysfunction in critically ill septic patients in the emergency department. J Clin Med 2019; 8 (02) 8
  • 94 Leisman D, Huang V, Zhou Q. et al. Delayed second dose antibiotics for patients admitted from the emergency department with sepsis: prevalence, risk factors, and outcomes. Crit Care Med 2017; 45 (06) 956-965
  • 95 Seymour CW, Kahn JM, Martin-Gill C. et al. Delays from first medical contact to antibiotic administration for sepsis. Crit Care Med 2017; 45 (05) 759-765
  • 96 Labelle A, Juang P, Reichley R. et al. The determinants of hospital mortality among patients with septic shock receiving appropriate initial antibiotic treatment*. Crit Care Med 2012; 40 (07) 2016-2021
  • 97 de Groot B, Ansems A, Gerling DH. et al. The association between time to antibiotics and relevant clinical outcomes in emergency department patients with various stages of sepsis: a prospective multi-center study. Crit Care 2015; 19: 194
  • 98 van Paridon BM, Sheppard C, , G GG, Joffe AR. Alberta Sepsis Network. Timing of antibiotics, volume, and vasoactive infusions in children with sepsis admitted to intensive care. Crit Care 2015; 19: 293
  • 99 Creedon JK, Vargas S, Asaro LA, Wypij D, Paul R, Melendez E. Timing of antibiotic administration in pediatric sepsis. Pediatr Emerg Care 2020; 36 (10) 464-467
  • 100 Alam N, Oskam E, Stassen PM. et al; PHANTASi Trial Investigators and the ORCA (Onderzoeks Consortium Acute Geneeskunde) Research Consortium the Netherlands. Prehospital antibiotics in the ambulance for sepsis: a multicentre, open label, randomised trial. Lancet Respir Med 2018; 6 (01) 40-50
  • 101 Sterling SA, Miller WR, Pryor J, Puskarich MA, Jones AE. The impact of timing of antibiotics on outcomes in severe sepsis and septic shock: a systematic review and meta-analysis. Crit Care Med 2015; 43 (09) 1907-1915
  • 102 Timsit JF, Bassetti M, Cremer O. et al. Rationalizing antimicrobial therapy in the ICU: a narrative review. Intensive Care Med 2019; 45 (02) 172-189
  • 103 IDSA Sepsis Task Force. Infectious Diseases Society of America (IDSA) Position Statement: why IDSA did not endorse the surviving sepsis campaign guidelines. Clin Infect Dis 2018; 66 (10) 1631-1635
  • 104 Klompas M, Calandra T, Singer M. Antibiotics for sepsis-finding the equilibrium. JAMA 2018; 320 (14) 1433-1434
  • 105 Marik PE, Farkas JD. The changing paradigm of sepsis: early diagnosis, early antibiotics, early pressors, and early adjuvant treatment. Crit Care Med 2018; 46 (10) 1690-1692
  • 106 Serafim R, Gomes JA, Salluh J, Póvoa P. A comparison of the Quick-SOFA and systemic inflammatory response syndrome criteria for the diagnosis of sepsis and prediction of mortality: a systematic review and meta-analysis. Chest 2018; 153 (03) 646-655
  • 107 Churpek MM, Snyder A, Han X. et al. Quick sepsis-related organ failure assessment, systemic inflammatory response syndrome, and early warning scores for detecting clinical deterioration in infected patients outside the intensive care unit. Am J Respir Crit Care Med 2017; 195 (07) 906-911
  • 108 Deis AS, Whiles BB, Brown AR, Satterwhite CL, Simpson SQ. Three-hour bundle compliance and outcomes in patients with undiagnosed severe sepsis. Chest 2018; 153 (01) 39-45
  • 109 Peltan ID, Mitchell KH, Rudd KE. et al. Prehospital care and emergency department door-to-antibiotic time in sepsis. Ann Am Thorac Soc 2018; 15 (12) 1443-1450
  • 110 Vattanavanit V, Buppodom T, Khwannimit B. Timing of antibiotic administration and lactate measurement in septic shock patients: a comparison between hospital wards and the emergency department. Infect Drug Resist 2018; 11: 125-132
  • 111 Petit J, Passerieux J, Maitre O. et al. Impact of a qSOFA-based triage procedure on antibiotic timing in ED patients with sepsis: a prospective interventional study. Am J Emerg Med 2020; 38 (03) 477-484
  • 112 Kim M, Song KH, Kim CJ. et al. Electronic alerts with automated consultations promote appropriate antimicrobial prescriptions. PLoS One 2016; 11 (08) e0160551
  • 113 Micek ST, Heard KM, Gowan M, Kollef MH. Identifying critically ill patients at risk for inappropriate antibiotic therapy: a pilot study of a point-of-care decision support alert. Crit Care Med 2014; 42 (08) 1832-1838
  • 114 Barlam TF, Cosgrove SE, Abbo LM. et al. Executive summary: implementing an antibiotic stewardship program: guidelines by the Infectious Diseases Society of America and the Society for Healthcare Epidemiology of America. Clin Infect Dis 2016; 62 (10) 1197-1202
  • 115 Garnacho-Montero J, Gutiérrez-Pizarraya A, Escoresca-Ortega A, Fernández-Delgado E, López-Sánchez JM. Adequate antibiotic therapy prior to ICU admission in patients with severe sepsis and septic shock reduces hospital mortality. Crit Care 2015; 19: 302
  • 116 Hitti EA, Lewin III JJ, Lopez J. et al. Improving door-to-antibiotic time in severely septic emergency department patients. J Emerg Med 2012; 42 (04) 462-469
  • 117 Goff DA, Bauer KA, Reed EE, Stevenson KB, Taylor JJ, West JE. Is the “low-hanging fruit” worth picking for antimicrobial stewardship programs?. Clin Infect Dis 2012; 55 (04) 587-592
  • 118 Messina AP, van den Bergh D, Goff DA. Antimicrobial stewardship with pharmacist intervention improves timeliness of antimicrobials across thirty-three hospitals in South Africa. Infect Dis Ther 2015; 4 (Suppl. 01) 5-14
  • 119 Kufel WD, Seabury RW, Meola GM, Darko W, Probst LA, Miller CD. Impact of premix antimicrobial preparation and time to administration in septic patients. CJEM 2018; 20 (04) 565-571
  • 120 Ferrer R, Martin-Loeches I, Phillips G. et al. Empiric antibiotic treatment reduces mortality in severe sepsis and septic shock from the first hour: results from a guideline-based performance improvement program. Crit Care Med 2014; 42 (08) 1749-1755
  • 121 Kumar A, Roberts D, Wood KE. et al. Duration of hypotension before initiation of effective antimicrobial therapy is the critical determinant of survival in human septic shock. Crit Care Med 2006; 34 (06) 1589-1596
  • 122 Kumar A, Ellis P, Arabi Y. et al; Cooperative Antimicrobial Therapy of Septic Shock Database Research Group. Initiation of inappropriate antimicrobial therapy results in a fivefold reduction of survival in human septic shock. Chest 2009; 136 (05) 1237-1248
  • 123 Ulldemolins M, Nuvials X, Palomar M, Masclans JR, Rello J. Appropriateness is critical. Crit Care Clin 2011; 27 (01) 35-51
  • 124 Balk RA, Kadri SS, Cao Z, Robinson SB, Lipkin C, Bozzette SA. Effect of procalcitonin testing on health-care utilization and costs in critically ill patients in the United States. Chest 2017; 151 (01) 23-33
  • 125 Antimicrobial resistance: tackling a crisis for the health and wealth of nations. Accessed July 10, 2021 at: https://bit.ly/36u4nKB
  • 126 Tabah A, Bassetti M, Kollef MH. et al. Antimicrobial de-escalation in critically ill patients: a position statement from a task force of the European Society of Intensive Care Medicine (ESICM) and European Society of Clinical Microbiology and Infectious Diseases (ESCMID) Critically Ill Patients Study Group (ESGCIP). Intensive Care Med 2020; 46 (02) 245-265
  • 127 Kalil AC, Metersky ML, Klompas M. et al. Management of adults with hospital-acquired and ventilator-associated pneumonia: 2016 Clinical Practice Guidelines by the Infectious Diseases Society of America and the American Thoracic Society. Clin Infect Dis 2016; 63 (05) e61-e111
  • 128 Tabah A, Cotta MO, Garnacho-Montero J. et al. A systematic review of the definitions, determinants, and clinical outcomes of antimicrobial de-escalation in the intensive care unit. Clin Infect Dis 2016; 62 (08) 1009-1017
  • 129 Ruiz J, Ramirez P, Gordon M. et al. Antimicrobial stewardship programme in critical care medicine: a prospective interventional study. Med Intensiva (Engl Ed) 2018; 42 (05) 266-273
  • 130 De Bus L, Depuydt P, Steen J. et al; DIANA Study Group. Antimicrobial de-escalation in the critically ill patient and assessment of clinical cure: the DIANA study. Intensive Care Med 2020; 46 (07) 1404-1417
  • 131 Martínez ML, Ferrer R, Torrents E. et al; Edusepsis Study Group. Impact of source control in patients with severe sepsis and septic shock. Crit Care Med 2017; 45 (01) 11-19
  • 132 Schein M, Marshall J. Source control for surgical infections. World J Surg 2004; 28 (07) 638-645
  • 133 Coopersmith CM, De Backer D, Deutschman CS. et al. Surviving sepsis campaign: research priorities for sepsis and septic shock. Crit Care Med 2018; 46 (08) 1334-1356
  • 134 De Backer D, Dorman T. Surviving sepsis guidelines: a continuous move toward better care of patients with sepsis. JAMA 2017; 317 (08) 807-808
  • 135 Chen AX, Simpson SQ, Pallin DJ. Sepsis guidelines. N Engl J Med 2019; 380 (14) 1369-1371
  • 136 Walsh D, Gekle R, Bramante R, Decena E, Raio C, Levy D. Emergency department sepsis huddles: achieving excellence for sepsis benchmarks in New York State. Am J Emerg Med 2020; 38 (02) 222-224