Unexplained mortality differences between septic shock trials: a systematic analysis of population characteristics and control-group mortality rates

Intensive Care Medicine

Volumn 44, Issue 3, 2018, Pages 311-322

  de Grooth, Harm Jan ^a   Postema, Jonne ^a   Loer, Stephan A ^a   Parienti, Jean Jacques ^b,c   Oudemans van Straaten, Heleen M ^a   Girbes, Armand R ^a  

^a VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^b CAEN UNIVERSITY HOSPITAL   (France)

^c UNIVERSITÉ DE ROUEN   (France)

Author keywords

Clinical trials; Heterogeneity; Machine learning; Meta research; Methodology; Septic shock

Indexed keywords

HYPERTENSIVE FACTOR; VASOCONSTRICTOR AGENT;

ANALYSIS OF VARIANCE; ARTIFICIAL VENTILATION; CLINICAL TRIAL (TOPIC); CONTROL GROUP; CREATININE BLOOD LEVEL; HUMAN; HYPOTENSION; INFECTION; MORTALITY RATE; POPULATION AND POPULATION RELATED PHENOMENA; POPULATION DISTRIBUTION; PREDICTIVE VALUE; REVIEW; SEPTIC SHOCK; SEQUENTIAL ORGAN FAILURE ASSESSMENT SCORE; STATISTICAL MODEL; SYSTEMATIC REVIEW; ADULT; CASE CONTROL STUDY; MALE; MORTALITY; ORGAN DYSFUNCTION SCORE; RANDOMIZED CONTROLLED TRIAL (TOPIC); SEPSIS;

ADULT; CASE-CONTROL STUDIES; HUMANS; MALE; ORGAN DYSFUNCTION SCORES; RANDOMIZED CONTROLLED TRIALS AS TOPIC; SEPSIS; SHOCK, SEPTIC; VASOCONSTRICTOR AGENTS;

EID: 85044058369     PISSN: 03424642     EISSN: 14321238     Source Type: Journal    
DOI: 10.1007/s00134-018-5134-8     Document Type: Review

References (98)

1. Bone RC, Balk RA, Cerra FB et al (1992) Definitions for sepsis and organ failure and guidelines for the use of innovative therapies in sepsis. The ACCP/SCCM Consensus Conference Committee. American College of Chest Physicians/Society of Critical Care Medicine. Chest 101:1644–1655
2. Levy MM, Fink MP, Marshall JC et al (2003) 2001 SCCM/ESICM/ACCP/ATS/SIS international sepsis definitions conference. Intensive Care Med 29:530–538. https://doi.org/10.1007/s00134-003-1662-x
3. Singer M, Deutschman CS, Seymour CW et al (2016) The third international consensus definitions for sepsis and septic shock (sepsis-3). JAMA 315:801–810. https://doi.org/10.1001/jama.2016.0287
4. Dellinger RP, Carlet JM, Masur H et al (2004) Surviving sepsis campaign guidelines for management of severe sepsis and septic shock. Intensive Care Med 30:536–555. https://doi.org/10.1007/s00134-004-2210-z
5. Shankar-Hari M, Phillips GS, Levy ML et al (2016) Developing a new definition and assessing new clinical criteria for septic shock: for the third international consensus definitions for sepsis and septic shock (sepsis-3). JAMA 315:775–787. https://doi.org/10.1001/jama.2016.0289
6. ARISE Investigators, ANZICS Clinical Trials Group, Peake SL et al (2014) Goal-directed resuscitation for patients with early septic shock. N Engl J Med 371:1496–1506. https://doi.org/10.1056/nejmoa1404380
7. Morelli A, Ertmer C, Westphal M et al (2013) Effect of heart rate control with esmolol on hemodynamic and clinical outcomes in patients with septic shock: a randomized clinical trial. JAMA 310:1683–1691. https://doi.org/10.1001/jama.2013.278477
8. Vincent J-L, Hall JB, Slutsky AS (2015) Ten big mistakes in intensive care medicine. Intensive Care Med 41:505–507. https://doi.org/10.1007/s00134-014-3570-7
9. Marshall JC (2014) Why have clinical trials in sepsis failed? Trends Mol Med 20:195–203. https://doi.org/10.1016/j.molmed.2014.01.007
10. Opal SM, Dellinger RP, Vincent J-L et al (2014) The next generation of sepsis clinical trial designs: what is next after the demise of recombinant human activated protein C? Crit Care Med 42:1714–1721. https://doi.org/10.1097/CCM.0000000000000325
11. Harhay MO, Wagner J, Ratcliffe SJ et al (2014) Outcomes and statistical power in adult critical care randomized trials. Am J Respir Crit Care Med 189:1469–1478. https://doi.org/10.1164/rccm.201401-0056CP
12. de Grooth HJ, Oudemans-van Straaten HM, Girbes AR (2016) Heterogeneity in a decade of septic shock RCTs: a systematic analysis of mortality outcomes. PROSPERO 2016 CRD42016049330. https://www.crd.york.ac.uk/PROSPERO/display_record.php?RecordID=49330. Accessed 3 Nov 2016
13. Moher D, Liberati A, Tetzlaff J et al (2009) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. BMJ 339:b2535
14. Jadad AR, Moore RA, Carroll D et al (1996) Assessing the quality of reports of randomized clinical trials: is blinding necessary? Control Clin Trials 17:1–12. https://doi.org/10.1016/0197-2456(95)00134-4
15. Deeks JJ, Higgins JPT, Altman DG (2011) Section 9.5: heterogeneity. Cochrane handbook for systematic reviews of interventions version 5.1.0 (updated March 2011)
16. IntHout J, Ioannidis JPA, Rovers MM, Goeman JJ (2016) Plea for routinely presenting prediction intervals in meta-analysis. BMJ Open 6:e010247. https://doi.org/10.1136/bmjopen-2015-010247
17. Breiman L, Friedman J, Olshen R, Stone C (1984) Classification and regression trees. CRC Press, Boca Raton, Florida, USA
18. Atkinson EJ, Therneau TM (2017) An introduction to recursive partitioning using the RPART routines. Mayo Found, Rochester, Minnesota, USA
19. Viechtbauer W (2010) Conducting meta-analyses in R with the metafor package. J Stat Softw. https://doi.org/10.18637/jss.v036.i03
20. Van Buuren S, Groothuis-Oudshoorn K (2011) mice: Multivariate imputation by chained equations in R. J Stat Softw 45:1–67. https://doi.org/10.18637/jss.v045.i03
21. Therneau T, Atkinson B, Ripley B (2017) rpart: recursive partitioning and regression trees. R Packag. version 4.1-11
22. Annane D, Vignon P, Renault A et al (2007) Norepinephrine plus dobutamine versus epinephrine alone for management of septic shock: a randomised trial. Lancet (London, England) 370:676–684. https://doi.org/10.1016/s0140-6736(07)61344-0
23. Annane D, Timsit J-F, Megarbane B et al (2013) Recombinant human activated protein C for adults with septic shock: a randomized controlled trial. Am J Respir Crit Care Med 187:1091–1097. https://doi.org/10.1164/rccm.201211-2020OC
24. Asfar P, Meziani F, Hamel J-F et al (2014) High versus low blood-pressure target in patients with septic shock. N Engl J Med 370:1583–1593. https://doi.org/10.1056/NEJMoa1312173
25. Bahloul M, Chaari A, Ben Mbarek MN et al (2012) Use of heptaminol hydrochloride for catecholamine weaning in septic shock. Am J Ther 19:e8–e17. https://doi.org/10.1097/MJT.0b013e3181e9b630
26. Chakraborty A, Mathur S, Dhunna R (2007) Comparison of norepinephrine and dopamine in the management of septic shock using impedance cardiography. Indian J Crit Care Med 11:186. https://doi.org/10.4103/0972-5229.37713
27. Chen C, Kollef MH (2015) Targeted fluid minimization following initial resuscitation in septic shock: a pilot study. Chest 148:1462–1469. https://doi.org/10.1378/chest.15-1525
28. Cicarelli DD, Vieira JE, Benseñor FEM (2007) Early dexamethasone treatment for septic shock patients: a prospective randomized clinical trial. São Paulo Med J (Rev Paul Med) 125:237–241
29. COIITSS Study Investigators, Annane D, Cariou A et al (2010) Corticosteroid treatment and intensive insulin therapy for septic shock in adults: a randomized controlled trial. JAMA 303:341–348. https://doi.org/10.1001/jama.2010.2
30. Dong W, Zhang G, Qu F (2015) Effects of Ringer’s sodium pyruvate solution on serum tumor necrosis factor-α and interleukin-6 upon septic shock. Pak J Med Sci 31:672–677. https://doi.org/10.12669/pjms.313.7170
31. Donnino MW, Andersen LW, Chase M et al (2016) Randomized, double-blind, placebo-controlled trial of thiamine as a metabolic resuscitator in septic shock: a pilot study. Crit Care Med 44:360–367. https://doi.org/10.1097/CCM.0000000000001572
32. Dubin A, Pozo MO, Casabella CA et al (2010) Comparison of 6% hydroxyethyl starch 130/0.4 and saline solution for resuscitation of the microcirculation during the early goal-directed therapy of septic patients. J Crit Care 25:659.e1–659.e8. https://doi.org/10.1016/j.jcrc.2010.04.007
33. Forceville X, Laviolle B, Annane D et al (2007) Effects of high doses of selenium, as sodium selenite, in septic shock: a placebo-controlled, randomized, double-blind, phase II study. Crit Care 11:R73. https://doi.org/10.1186/cc5960
34. Garg M, Sen J, Goyal S, Chaudhry D (2016) Comparative evaluation of central venous pressure and sonographic inferior vena cava variability in assessing fluid responsiveness in septic shock. Indian J Crit Care Med 20:708–713. https://doi.org/10.4103/0972-5229.195706
35. Gordon AC, Mason AJ, Perkins GD et al (2014) The interaction of vasopressin and corticosteroids in septic shock: a pilot randomized controlled trial. Crit Care Med 42:1325–1333. https://doi.org/10.1097/CCM.0000000000000212
36. Gordon AC, Mason AJ, Thirunavukkarasu N et al (2016) Effect of early vasopressin vs norepinephrine on kidney failure in patients with septic shock: the VANISH randomized clinical trial. JAMA 316:509–518. https://doi.org/10.1001/jama.2016.10485
37. Hajjej Z, Meddeb B, Sellami W et al (2017) Effects of levosimendan on cellular metabolic alterations in patients with septic shock: a randomized controlled pilot study. Shock 48:307–312. https://doi.org/10.1097/SHK.0000000000000851
38. Hjortrup PB, Haase N, Bundgaard H et al (2016) Restricting volumes of resuscitation fluid in adults with septic shock after initial management: the CLASSIC randomised, parallel-group, multicentre feasibility trial. Intensive Care Med 42:1695–1705. https://doi.org/10.1007/s00134-016-4500-7
39. Huh JW, Choi H-S, Lim C-M et al (2011) Low-dose hydrocortisone treatment for patients with septic shock: a pilot study comparing 3 days with 7days. Respirology 16:1088–1095. https://doi.org/10.1111/j.1440-1843.2011.02018.x
40. Hyvernat H, Barel R, Gentilhomme A et al (2016) Effects of increasing hydrocortisone to 300 mg per day in the treatment of septic shock: a pilot study. Shock 46:498–505. https://doi.org/10.1097/SHK.0000000000000665
41. Juffermans NP, Vervloet MG, Daemen-Gubbels CRG et al (2010) A dose-finding study of methylene blue to inhibit nitric oxide actions in the hemodynamics of human septic shock. Nitric Oxide 22:275–280. https://doi.org/10.1016/j.niox.2010.01.006
42. Li M-Q, Pan C-G, Wang X-M et al (2015) Effect of the shenfu injection combined with early goal-directed therapy on organ functions and outcomes of septic shock patients. Cell Biochem Biophys 72:807–812. https://doi.org/10.1007/s12013-015-0537-4
43. Li Y, Zhang X, Lin P et al (2016) Effects of shenfu injection in the treatment of septic shock patients: a multicenter, controlled, randomized, open-label trial. Evid Based Complement Alternat Med 2016:2565169. https://doi.org/10.1155/2016/2565169
44. Lin S-M, Huang C-D, Lin H-C et al (2006) A modified goal-directed protocol improves clinical outcomes in intensive care unit patients with septic shock: a randomized controlled trial. Shock 26:551–557. https://doi.org/10.1097/01.shk.0000232271.09440.8f
45. Livigni S, Bertolini G, Rossi C et al (2014) Efficacy of coupled plasma filtration adsorption (CPFA) in patients with septic shock: a multicenter randomised controlled clinical trial. BMJ Open 4:e003536. https://doi.org/10.1136/bmjopen-2013-003536
46. Loisa P, Parviainen I, Tenhunen J et al (2007) Effect of mode of hydrocortisone administration on glycemic control in patients with septic shock: a prospective randomized trial. Crit Care 11:R21. https://doi.org/10.1186/cc5696
47. Lu N-F, Zheng R-Q, Lin H et al (2015) Improved sepsis bundles in the treatment of septic shock: a prospective clinical study. Am J Emerg Med 33:1045–1049. https://doi.org/10.1016/j.ajem.2015.04.031
48. Lv Q, Gu X, Chen Q et al (2017) Early initiation of low-dose hydrocortisone treatment for septic shock in adults: a randomized clinical trial. Am J Emerg Med 35:1810–1814. https://doi.org/10.1016/j.ajem.2017.06.004
49. McIntyre LA, Fergusson D, Cook DJ et al (2008) Fluid resuscitation in the management of early septic shock (FINESS): a randomized controlled feasibility trial. Can J Anaesth (J Can d’anesthésie) 55:819–826. https://doi.org/10.1007/bf03034053
50. Memiş D, Kargi M, Sut N (2009) Effects of propofol and dexmedetomidine on indocyanine green elimination assessed with LIMON to patients with early septic shock: a pilot study. J Crit Care 24:603–608. https://doi.org/10.1016/j.jcrc.2008.10.005
51. Merouani M, Guignard B, Vincent F et al (2008) Norepinephrine weaning in septic shock patients by closed loop control based on fuzzy logic. Crit Care 12:R155. https://doi.org/10.1186/cc7149
52. Morelli A, Lange M, Ertmer C et al (2007) Glibenclamide dose response in patients with septic shock: effects on norepinephrine requirements, cardiopulmonary performance, and global oxygen transport. Shock 28:530–535. https://doi.org/10.1097/shk.0b013e3180556a3c
53. Morelli A, Ertmer C, Rehberg S et al (2009) Continuous terlipressin versus vasopressin infusion in septic shock (TERLIVAP): a randomized, controlled pilot study. Crit Care 13:R130. https://doi.org/10.1186/cc7990
54. Morelli A, Ertmer C, Rehberg S et al (2008) Phenylephrine versus norepinephrine for initial hemodynamic support of patients with septic shock: a randomized, controlled trial. Crit Care 12:R143. https://doi.org/10.1186/cc7121
55. Morelli A, Ertmer C, Lange M et al (2008) Effects of short-term simultaneous infusion of dobutamine and terlipressin in patients with septic shock: the DOBUPRESS study. Br J Anaesth 100:494–503. https://doi.org/10.1093/bja/aen017
56. Morelli A, Donati A, Ertmer C et al (2010) Levosimendan for resuscitating the microcirculation in patients with septic shock: a randomized controlled study. Crit Care 14:R232. https://doi.org/10.1186/cc9387
57. Mouncey PR, Osborn TM, Power GS et al (2015) Trial of early, goal-directed resuscitation for septic shock. N Engl J Med 372:1301–1311. https://doi.org/10.1056/NEJMoa1500896
58. Ngaosuwan K, Ounchokdee K, Chalermchai T (2017) Clinical outcomes of minimized hydrocortisone dosage of 100 mg/day on lower occurrence of hyperglycemia in septic shock patients. Shock. https://doi.org/10.1097/SHK.0000000000001061
59. Palizas F, Dubin A, Regueira T et al (2009) Gastric tonometry versus cardiac index as resuscitation goals in septic shock: a multicenter, randomized, controlled trial. Crit Care 13:R44. https://doi.org/10.1186/cc7767
60. Patel GP, Grahe JS, Sperry M et al (2010) Efficacy and safety of dopamine versus norepinephrine in the management of septic shock. Shock 33:375–380. https://doi.org/10.1097/SHK.0b013e3181c6ba6f
61. Payen DM, Guilhot J, Launey Y et al (2015) Early use of polymyxin B hemoperfusion in patients with septic shock due to peritonitis: a multicenter randomized control trial. Intensive Care Med 41:975–984. https://doi.org/10.1007/s00134-015-3751-z
62. Investigators ProCESS, Yealy DM, Kellum JA et al (2014) A randomized trial of protocol-based care for early septic shock. N Engl J Med 370:1683–1693. https://doi.org/10.1056/NEJMoa1401602
63. Puskarich MA, Kline JA, Krabill V et al (2014) Preliminary safety and efficacy of l-carnitine infusion for the treatment of vasopressor-dependent septic shock: a randomized control trial. JPEN J Parenter Enter Nutr 38:736–743. https://doi.org/10.1177/0148607113495414
64. Quenot J-P, Binquet C, Vinsonneau C et al (2015) Very high volume hemofiltration with the Cascade system in septic shock patients. Intensive Care Med 41:2111–2120. https://doi.org/10.1007/s00134-015-4056-y
65. Ranieri VM, Thompson BT, Barie PS et al (2012) Drotrecogin alfa (activated) in adults with septic shock. N Engl J Med 366:2055–2064. https://doi.org/10.1056/NEJMoa1202290
66. Richard J-C, Bayle F, Bourdin G et al (2015) Preload dependence indices to titrate volume expansion during septic shock: a randomized controlled trial. Crit Care 19:5. https://doi.org/10.1186/s13054-014-0734-3
67. Russell JA, Vincent J-L, Kjølbye AL et al (2017) Selepressin, a novel selective vasopressin V1A agonist, is an effective substitute for norepinephrine in a phase IIa randomized, placebo-controlled trial in septic shock patients. Crit Care 21:213. https://doi.org/10.1186/s13054-017-1798-7
68. Russell JA, Walley KR, Singer J et al (2008) Vasopressin versus norepinephrine infusion in patients with septic shock. N Engl J Med 358:877–887. https://doi.org/10.1056/NEJMoa067373
69. Schmoelz M, Schelling G, Dunker M, Irlbeck M (2006) Comparison of systemic and renal effects of dopexamine and dopamine in norepinephrine-treated septic shock. J Cardiothorac Vasc Anesth 20:173–178. https://doi.org/10.1053/j.jvca.2005.10.016
70. Schortgen F, Clabault K, Katsahian S et al (2012) Fever control using external cooling in septic shock: a randomized controlled trial. Am J Respir Crit Care Med 185:1088–1095. https://doi.org/10.1164/rccm.201110-1820OC
71. Seguin P, Laviolle B, Guinet P et al (2006) Dopexamine and norepinephrine versus epinephrine on gastric perfusion in patients with septic shock: a randomized study [NCT00134212]. Crit Care 10:R32. https://doi.org/10.1186/cc4827
72. Shum HP, Leung YW, Lam SM et al (2014) Alteco endotoxin hemoadsorption in Gram-negative septic shock patients. Indian J Crit Care Med 18:783–788. https://doi.org/10.4103/0972-5229.146305
73. Singh RK, Agarwal V, Baronia AK et al (2017) The effects of atorvastatin on inflammatory responses and mortality in septic shock: a single-center, randomized controlled trial. Indian J Crit Care Med 21:646–654. https://doi.org/10.4103/ijccm.IJCCM_474_16
74. Sprung CL, Annane D, Keh D et al (2008) Hydrocortisone therapy for patients with septic shock. N Engl J Med 358:111–124. https://doi.org/10.1056/NEJMoa071366
75. Stephens DP, Thomas JH, Higgins A et al (2008) Randomized, double-blind, placebo-controlled trial of granulocyte colony-stimulating factor in patients with septic shock. Crit Care Med 36:448–454. https://doi.org/10.1097/01.CCM.0B013E318161E480
76. Torraco A, Carrozzo R, Piemonte F et al (2014) Effects of levosimendan on mitochondrial function in patients with septic shock: a randomized trial. Biochimie 102:166–173. https://doi.org/10.1016/j.biochi.2014.03.006
77. Trof RJ, Beishuizen A, Cornet AD et al (2012) Volume-limited versus pressure-limited hemodynamic management in septic and nonseptic shock. Crit Care Med 40:1177–1185. https://doi.org/10.1097/CCM.0b013e31823bc5f9
78. Trzeciak S, Glaspey LJ, Dellinger RP et al (2014) Randomized controlled trial of inhaled nitric oxide for the treatment of microcirculatory dysfunction in patients with sepsis. Crit Care Med 42:2482–2492. https://doi.org/10.1097/CCM.0000000000000549
79. van Genderen ME, Engels N, van der Valk RJP et al (2015) Early peripheral perfusion-guided fluid therapy in patients with septic shock. Am J Respir Crit Care Med 191:477–480. https://doi.org/10.1164/rccm.201408-1575LE
80. van Haren FMP, Sleigh J, Boerma EC et al (2012) Hypertonic fluid administration in patients with septic shock: a prospective randomized controlled pilot study. Shock 37:268–275. https://doi.org/10.1097/SHK.0b013e31823f152f
81. Venkatesh B, Finfer S, Cohen J et al (2018) Adjunctive glucocorticoid therapy in patients with septic shock. N Engl J Med NEJMoa1705835. https://doi.org/10.1056/nejmoa1705835
82. Xu Q, Yan J, Cai G et al (2014) Effect of two volume responsiveness evaluation methods on fluid resuscitation and prognosis in septic shock patients. Chin Med J (Engl) 127:483–487. https://doi.org/10.3760/cma.j.issn.0366-6999.20131830
83. Yu T, Peng X, Liu L et al (2015) Propofol increases preload dependency in septic shock patients. J Surg Res 193:849–855. https://doi.org/10.1016/j.jss.2014.08.050
84. Zhou X, Liu D, Su L et al (2017) Use of stepwise lactate kinetics-oriented hemodynamic therapy could improve the clinical outcomes of patients with sepsis-associated hyperlactatemia. Crit Care 21:33. https://doi.org/10.1186/s13054-017-1617-1
85. Kaukonen K-M, Bailey M, Suzuki S et al (2014) Mortality related to severe sepsis and septic shock among critically ill patients in Australia and New Zealand, 2000–2012. JAMA 311:1308–1316. https://doi.org/10.1001/jama.2014.2637
86. Gaieski DF, Edwards JM, Kallan MJ, Carr BG (2013) Benchmarking the incidence and mortality of severe sepsis in the United States. Crit Care Med 41:1167–1174. https://doi.org/10.1097/CCM.0b013e31827c09f8
87. Klein Klouwenberg PMC, Ong DSY, Bonten MJM, Cremer OL (2012) Classification of sepsis, severe sepsis and septic shock: the impact of minor variations in data capture and definition of SIRS criteria. Intensive Care Med 38:811–819. https://doi.org/10.1007/s00134-012-2549-5
88. Féry-Lemonnier E, Landais P, Loirat P et al (1995) Evaluation of severity scoring systems in ICUs—translation, conversion and definition ambiguities as a source of inter-observer variability in Apache II, SAPS and OSF. Intensive Care Med 21:356–360. https://doi.org/10.1007/BF01705416
89. Pettilä V, Hjortrup PB, Jakob SM et al (2016) Control groups in recent septic shock trials: a systematic review. Intensive Care Med 42:1912–1921. https://doi.org/10.1007/s00134-016-4444-y
90. Porter ME, Larsson S, Lee TH (2016) Standardizing patient outcomes measurement. N Engl J Med 374:504–506. https://doi.org/10.1056/NEJMp1511701
91. Myles PS, Grocott MPW, Boney O et al (2016) Standardizing end points in perioperative trials: towards a core and extended outcome set. Br J Anaesth 116:586–589. https://doi.org/10.1093/bja/aew066
92. Vincent J, Martin-Loeches I, Annane D (2016) What patient data should be collected in this randomized controlled trial in sepsis? Intensive Care Med 42:2011–2013. https://doi.org/10.1007/s00134-016-4560-8
93. Investigators PRISM, Rowan KM, Angus DC et al (2017) Early, goal-directed therapy for septic shock—a patient-level meta-analysis. N Engl J Med 376:2223–2234. https://doi.org/10.1056/NEJMoa1701380
94. Shankar-Hari M, Harrison DA, Rowan KM (2016) Differences in impact of definitional elements on mortality precludes international comparisons of sepsis epidemiology—a cohort study illustrating the need for standardized reporting. Crit Care Med 44:2223–2230. https://doi.org/10.1097/CCM.0000000000001876
95. Martin GS, Mannino DM, Eaton S, Moss M (2003) The epidemiology of sepsis in the United States from 1979 through 2000. N Engl J Med 348:1546–1554. https://doi.org/10.1056/NEJMoa022139
96. Ferreira FL, Bota DP, Bross A et al (2001) Serial evaluation of the SOFA score to predict outcome in critically ill patients. JAMA 286:1754–1758. https://doi.org/10.1001/jama.286.14.1754
97. Minne L, Abu-Hanna A, de Jonge E (2008) Evaluation of SOFA-based models for predicting mortality in the ICU: a systematic review. Crit Care 12:R161. https://doi.org/10.1186/cc7160
98. Kempker JA, Martin GS (2016) Does sepsis case mix heterogeneity prevent outcome comparisons? Crit Care Med 44:2288–2289. https://doi.org/10.1097/CCM.0000000000001933