Effects of red blood cell storage time on transfused patients in the ICU—protocol for a systematic review

Acta Anaesthesiologica Scandinavica

Volumn 61, Issue 10, 2017, Pages 1384-1397

  Rygard S L ^a   Jonsson, A B ^a   Madsen, M B ^a   Perner, A ^a,b   Holst, L B ^a   Johansson, P I ^a   Wetterslev, J ^a,b  

^a International Center for Research and Research Training in Endocrine Disruption of Male Reproduction and Child Health   (Denmark)

^b Centre for Research in Intensive Care   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

BLOOD STORAGE; BLOOD TRANSFUSION; CLINICAL PROTOCOL; CRITICALLY ILL PATIENT; DATA SYNTHESIS; ERYTHROCYTE PRESERVATION; ERYTHROCYTE TRANSFUSION; HUMAN; INFORMATION PROCESSING; INTENSIVE CARE UNIT; META ANALYSIS; OBSERVATIONAL STUDY; OUTCOME ASSESSMENT; PRIORITY JOURNAL; QUALITY CONTROL; REVIEW; RISK ASSESSMENT; SEQUENCE ANALYSIS; SEQUENTIAL ANALYSIS; SYSTEMATIC REVIEW; TIME FACTOR;

BLOOD PRESERVATION; CLINICAL PROTOCOLS; ERYTHROCYTE TRANSFUSION; HUMANS; INTENSIVE CARE UNITS; OUTCOME ASSESSMENT (HEALTH CARE); TIME FACTORS;

EID: 85035233644     PISSN: 00015172     EISSN: 13996576     Source Type: Journal    
DOI: 10.1111/aas.12991     Document Type: Review

References (112)

1. Vincent JL, Baron J-F, Reinhart K, Gattinoni L, Thijs L, Webb A, Meier-Hellmann A, Nollet G, Peres-Bota D. Anemia and blood transfusion in critically ill patients. JAMA 2002; 288: 1499–507.
2. Corwin HL, Gettinger A, Pearl RG, Fink MP, Levy MM, Abraham E, MacIntyre NR, Shabot M, Duh M, Shapiro MJ. The CRIT Study: anemia and blood transfusion in the critically ill - Current clinical practice in the United States. Crit Care Med 2004; 32: 39–52.
3. Nguyen BV, Bota DP, Mélot C, Vincent J-L. Time course of hemoglobin concentrations in nonbleeding intensive care unit patients. Crit Care Med 2003; 31: 406–10.
4. Walsh TS, Lee RJ, Maciver CR, Garrioch M, MacKirdy F, Binning AR, Cole S, McClelland DB. Anemia during and at discharge from intensive care: the impact of restrictive blood transfusion practice. Intensive Care Med 2006; 32: 100–9.
5. Bateman AP, McArdle F, Walsh TS. Time course of anemia during six months follow up following intensive care discharge and factors associated with impaired recovery of erythropoiesis. Crit Care Med 2009; 37: 1906–12.
6. Corwin HL, Parsonnet K, Gettinger A. RBC transfusion in the ICU – is there a reason? CHEST J 1995; 108: 767–71.
7. von Ahsen N, Müller C, Serke S, Frei U, Eckardt K-U. Important role of nondiagnostic blood loss and blunted erythropoietic response in the anemia of medical intensive care patients. Crit Care Med 1999; 27: 2630–9.
8. Scharte M, Fink MP. Red blood cell physiology in critical illness. Crit Care Med 2003; 31: S651–7.
9. Rogiers P, Zhang H, Leeman M, Nagler J, Neels H, Mélot C, Vincent JL. Erythropoietin response is blunted in critically ill patients. Intensive Care Med 1997; 23: 159–62.
10. Rodriguez RM, Corwin HL, Gettinger A, Corwin MJ, Gubler D, Pearl RG. Nutritional deficiencies and blunted erythropoietin response as causes of the anemia of critical illness. J Crit Care 2001; 16: 36–41.
11. Heming N, Montravers P, Lasocki S. Iron deficiency in critically ill patients: highlighting the role of hepcidin. Crit Care 2011; 15: 210.
12. Thein M, Ershler WB, Artz AS, Tecson J, Robinson BE, Rothstein G, Liede A, Gylys-Colwell I, Lu ZJ, Robbins S. Diminished quality of life and physical function in community-dwelling elderly with anemia. Medicine 2009; 88: 107–14.
13. Lucca U, Tettamanti M, Mosconi P, Apolone G, Gandini F, Nobili A, Tallone MV, Detoma P, Giacomin A, Clerico M, Tempia P, Guala A, Fasolo G, Riva E. Association of mild anemia with cognitive, functional, mood and quality of life outcomes in the elderly: the “health and anemia” study. PLoS ONE 2008; 3: e1920.
14. Ludwig H, Van Belle S, Barrett-Lee P, Birgegård G, Bokemeyer C, Gascón P, Kosmidis P, Krzakowski M, Nortier J, Olmi P, Schneider M, Schrijvers D. The European Cancer Anaemia Survey (ECAS): a large, multinational, prospective survey defining the prevalence, incidence, and treatment of anaemia in cancer patients. Eur J Cancer 2004; 40: 2293–306.
15. Ezekowitz JA, McAlister FA, Armstrong PW. Anemia is common in heart failure and is associated with poor outcomes: insights from a cohort of 12 065 patients with new-onset heart failure. Circulation 2003; 107: 223–5.
16. Horwich TB, Fonarow GC, Hamilton MA, MacLellan WR, Borenstein J. Anemia is associated with worse symptoms, greater impairment in functional capacity and a significant increase in mortality in patients with advanced heart failure. J Am Coll Cardiol 2002; 39: 1780–6.
17. Cuthbertson BH, Roughton S, Jenkinson D, Maclennan G, Vale L. Quality of life in the five years after intensive care: a cohort study. Crit Care 2010; 14: R6.
18. Hayden SJ, Albert TJ, Watkins TR, Swenson ER. Anemia in critical illness: insights into etiology, consequences, and management. Am J Respir Crit Care Med 2012; 185: 1049–57.
19. Prescott HC, Osterholzer JJ, Langa KM, Angus DC, Iwashyna TJ. Late mortality after sepsis: propensity matched cohort study. BMJ 2016; 353: i2375.
20. Yende S, Austin S, Rhodes A, Finfer SR, Opal SM, Thompson BT, Bozza FA, LaRosa SP, Ranieri VM, Angus DC. Long-term quality of life among survivors of severe sepsis. Crit Care Med 2016; 44: 1461–7.
21. Pieracci FM, Stovall RT, Jaouen B, Rodil M, Cappa A, Burlew CC, Holena DN, Maier R, Berry S, Jurkovich J, Moore EE. A multicenter, randomized clinical trial of IV iron supplementation for anemia of traumatic critical illness. Crit Care Med 2014; 42: 1–10.
22. Litton E, Baker S, Erber WN, Farmer S, Ferrier J, French C, Gummer J, Hawkins D, Higgins A, Hofmann A, De Keulenaer B, McMorrow J, Olynyk JK, Richards T, Towler S, Trengove R, Webb S. Intravenous iron or placebo for anaemia in intensive care: the IRONMAN multicentre randomized blinded trial. Intensive Care Med 2016; 42: 1715–22.
23. Corwin HL, Gettinger A, Pearl RG, Fink MP, Levy MM, Shapiro MJ, Corwin MJ, Colton T. Efficacy of recombinant human erythropoietin in critically Ill patients. JAMA 2002; 288: 2827–35.
24. Silver M, Corwin MJ, Bazan A, Gettinger A, Enny C, Corwin HL. Efficacy of recombinant human erythropoietin in critically ill patients admitted to a long-term acute care facility: a randomized, double-blind, placebo-controlled trial. Crit Care Med 2006; 34: 2310–6.
25. Corwin HL, Gettinger A, Fabian T, May AK, Pearl RG, Heard S, An R, Bowers P, Burton P, Klausner M, Corwin MJ. Efficacy and safety of epoetin alfa in critically Ill patients. N Engl J Med 2007; 357: 965–76.
26. Sun CC, Vaja V, Babitt J, Lin HY. Targeting the hepcidin-ferroportin axis to develop new treatment strategies for anemia of chronic disease and anemia of inflammation. Am J Hematol 2012; 87: 392–400.
27. Zarychanski R, Turgeon AF, McIntyre LA, Fergusson DA. Erythropoietin-receptor agonists in critically ill patients: a meta-analysis of randomized controlled trials. Can Med Assoc J 2007; 177: 725–34.
28. Zhao C, Lin Z, Luo Q, Xia X, Yu X, Huang F. Efficacy and safety of erythropoietin to prevent acute kidney injury in patients with critical illness or perioperative care: a systematic review and meta-analysis of randomized controlled trials. J Cardiovasc Pharmacol 2015; 65: 593–600.
29. Shah A, Roy NB, McKechnie S, Doree C, Fisher SA, Stanworth SJ. Iron supplementation to treat anaemia in adult critical care patients: a systematic review and meta-analysis. Crit Care 2016; 20: 306.
30. Zarychanski R, Doucette S, Fergusson D, Roberts D, Houston DS, Sharma S, Gulati H, Kumar A. Early intravenous unfractionated heparin and mortality in septic shock. Crit Care Med 2008; 36: 2973–9.
31. Perner A, Haase N, Guttormsen AB, Tenhunen J, Klemenzson G, Åneman A, Madsen KR, Møller MH, Elkjær JM, Poulsen LM, Bendtsen A, Winding R, Steensen M, Berezowicz P, Søe-Jensen P, Bestle M, Strand K, Wiis J, White JO, Thornberg KJ, Quist L, Nielsen J, Andersen LH, Holst LB, Thormar K, Kjældgaard A-L, Fabritius ML, Mondrup F, Pott FC, Møller TP, Winkel P, Wetterslev J. Hydroxyethyl starch 130/0.42 versus Ringer's acetate in severe sepsis. N Engl J Med 2012; 367: 124–34.
32. Department of Health and Human Services. The 2011 National Blood Collection and Utilization Survey Report, 2011. Available at: https://www.aabb.org/research/hemovigilance/bloodsurvey/Documents/11-nbcus-report.pdf (accessed 1 May 2017).
33. Walsh TS, Garrioch M, Madver C, Lee RJ, Mackirdy F, Mcclelland DB, Kinsella J, Wallisfor C. Red cell requirements for intensive care units adhering to evidence-based transfusion guidelines. Transfusion 2004; 44: 1405–11.
34. Westbrook A, Pettilä V, Nichol A, Bailey MJ, Syres G, Murray L, Bellomo R, Wood E, Phillips LE, Street A, French C, Orford N, Santamaria J, Cooper DJ. Transfusion practice and guidelines in Australian and New Zealand intensive care units. Intensive Care Med 2010; 36: 1138–46.
35. Norgaard A, De Lichtenberg TH, Nielsen J, Johansson PI. Monitoring compliance with transfusion guidelines in hospital departments by electronic data capture. Blood Transfus 2014; 12: 509–19.
36. National Blood Authority. Patient blood management guidelines: module 4 – critical care, 1–16. Available at: www.nba.gov.au 2012. https://doi.org/10.1186/cc9969.
37. Centre NCG. Blood transfusion – NICE guideline NG24, Methods evidence and recommendations. National Institute For Health and Care Excellence 2015. Available at: //www.ncbi.nlm.nih.gov/pubmed/26632625 (accessed 1 May 2017).
38. Carson JL, Guyatt G, Heddle NM, Grossman BJ, Cohn CS, Fung MK, Gernsheimer T, Holcomb JB, Kaplan LJ, Katz LM, Peterson N, Ramsey G, Rao SV, Roback JD, Shander A, Tobian AAR. Clinical practice guidelines from the AABB – red blood CEll transfusion threshold and storage. JAMA 2016; 316: 2025–35.
39. Dansk Selskab forfor Klinisk Immunologi. Transfusionsmedicinske standarder, 2016. Available at: http://tms-online.dk/files/TMS.3.5.2014.pdf (accessed 1 May 2017).
40. American Association of Blood Banks. Circular of information for the use of human blood and blood components, 2013. Available at: http://www.aabb.org/tm/coi/Documents/coi1113.pdf (accessed 1 May 2017).
41. Lægemiddelstyrelsen. Bekendtgørelse om kvalitets- og sikkerhedskrav til blodbankvirksomhed. Available at: https://www.retsinformation.dk/Forms/R0710.aspx?id=10174 2005 (accessed 1 May 2017).
42. Whitaker B, Rajbhandary S, Kleinman S, Harris A, Kamani N. Trends in United States blood collection and transfusion: results from the 2013 AABB Blood Collection, Utilization, and Patient Blood Management Survey. Transfusion 2016; 56: 2173–83.
43. Dzik S. Leukodepletion blood filters: filter design and mechanisms of leukocyte removal. Transfus Med Rev 1993; 7: 65–77.
44. Shapiro MJ. To filter blood or universal leukoreduction: what is the answer? Crit Care 2004; 8(Suppl 2): S27–30.
45. Vamvakas EC, Blajchman MA. Transfusion-related mortality: the ongoing risks of allogeneic blood transfusion and the available strategies for their prevention. Blood 2009; 113: 3406–17.
46. Garraud O, Tariket S, Sut C, Haddad A, Aloui C, Chakroun T, Laradi S, Cognasse F. Transfusion as an Inflammation Hit: knowns and Unknowns. Front Immunol 2016; 7: 1–10.
47. Muszynski JA, Spinella PC, Cholette JM, Acker JP, Hall MW, Juffermans NP, Kelly DP, Blumberg N, Nicol K, Liedel J, Doctor A, Remy KE, Tucci M, Lacroix J, Norris PJ. Transfusion-related immunomodulation: review of the literature and implications for pediatric critical illness. Transfusion 2017; 57: 195–206.
48. Hebert P, Wells G, Blajchman M, Marshall J, Martin C, Pagliarello G, Tweeddale M, Schweitzer I, Yetisir E. A Multicenter, randomized, controlled clinical trial of transfusion requirements in critical care. N Engl J Med 1999; 340: 409–17.
49. Marik PE, Corwin HL. Efficacy of red blood cell transfusion in the critically ill: a systematic review of the literature. Crit Care Med 2008; 36: 2667–74.
50. Chatterjee S, Wetterslev J, Sharma A, Lichstein E, Mukherjee D. Association of blood transfusion with increased mortality in myocardial infarction: a meta-analysis and diversity-adjusted study sequential analysis. JAMA Intern Med 2013; 173: 132–9.
51. Carson JL, Terrin ML, Noveck H, Sanders DW, Chaitman BR. Liberal or restrictive transfusion in high-risk patients after hip surgery. N Engl J Med 2011; 365: 2453–62.
52. Holst LB, Haase N, Wetterslev J, Wernerman J, Guttormsen AB, Karlsson S, Johansson PI, Aneman A, Vang ML, Winding R, Nebrich L, Nibro HL, Rasmussen BS, Lauridsen JRM, Nielsen JS, Oldner A, Pettila V, Cronhjort MB, Andersen LH, Pedersen UG, Reiter N, Wiis J, White JO, Russell L, Thornberg KJ, Hjortrup PB, Muller RG, Moller MH, Steensen M, Tjader I, Kilsand K, Odeberg-Wernerman S, Sjobo B, Bundgaard H, Thyo MA, Lodahl D, Maerkedahl R, Albeck C, Illum D, Kruse M, Winkel P, Perner A. Lower versus higher hemoglobin threshold for transfusion in septic shock. N Engl J Med 2014; 371: 1381–91.
53. Holst LB, Petersen MW, Haase N, Perner A, Wetterslev J. Restrictive versus liberal transfusion strategy for red blood cell transfusion: systematic review of randomised trials with meta-analysis and trial sequential analysis. BMJ 2015; 350: h1354.
54. Carson JL, Sieber F, Cook DR, Hoover DR, Noveck H, Chaitman BR, Fleisher L, Beaupre L, Macaulay W, Rhoads GG, Paris B, Zagorin A, Sanders DW, Zakriya KJ, Magaziner J. Liberal versus restrictive blood transfusion strategy: 3-year survival and cause of death results from the FOCUS randomised controlled trial. Lancet 2015; 385: 1183–9.
55. Rygård SL, Holst LB, Wetterslev J, Winkel P, Johansson PI, Wernerman J, Guttormsen AB, Karlsson S, Perner A. Long-term outcomes in patients with septic shock transfused at a lower versus a higher haemoglobin threshold: the TRISS randomised, multicentre clinical trial. Intensive Care Med 2016; 42: 1685–94.
56. Hebert PC, Fergusson D, Blajchman MA, Wells GA, Kmetic A, Devine D. Clinical outcomes following institution of the Canadian Universal Leukoreduction Program for Red Blood Cell Transfusions. JAMA 2003; 289: 1941–9.
57. Blumberg N, Zhao H, Wang H, Messing S, Heal JM, Lyman GH. The intention-to-treat principle in clinical trials and meta-analyses of leukoreduced blood transfusions in surgical patients. Transfusion 2007; 47: 573–81.
58. Lannan KL, Sahler J, Spinelli SL, Phipps RP, Blumberg N. Transfusion immunomodulation – the case for leukoreduced and (perhaps) washed transfusions. Blood Cells Mol Dis 2013; 50: 61–8.
59. Wolfe LC. The membrane and the lesions of storage in preserved red cells. Transfusion 1985; 25: 185–203.
60. Berezina TL, Zaets SB, Morgan C, Spillert CR, Kamiyama M, Spolarics Z, Deitch EA, Machiedo GW. Influence of storage on red blood cell rheological properties. J Surg Res 2002; 102: 6–12.
61. Bordbar A, Johansson PI, Paglia G, Harrison SJ, Wichuk K, Magnusdottir M, Valgeirsdottir S, Gybel-Brask M, Ostrowski SR, Palsson S, Rolfsson O, Sigurjonsson OE, Hansen MB, Gudmundsson S, Palsson BO. Identified metabolic signature for assessing red blood cell unit quality is associated with endothelial damage markers and clinical outcomes. Transfusion 2016; 56: 852–62.
62. Tinmouth A, Chin-Yee I. The clinical consequences of the red cell storage lesion. Transfus Med Rev 2001; 15: 91–107.
63. Valtis DJ, Kennedy A. Defective gas-transport function of stored red blood-cells. Lancet 1954; 266: 119–25.
64. Marik PE, Sibbald WJ. Effect of stored-blood transfusion on oxygen dilevery in patients with sepsis. JAMA 1993; 269: 3024–9.
65. Anniss AM, Sparrow RL. Storage duration and white blood cell content of red blood cell (RBC) products increases adhesion of stored RBCs to endothelium under flow conditions. Transfusion 2006; 46: 1561–7.
66. Neuman R, Hayek S, Rahman A, Poole JC, Menon V, Sher S, Newman JL, Karatela S, Polhemus D, Lefer DJ, De Staercke C, Hooper C, Quyyumi AA, Roback JD. Effects of storage-aged red blood cell transfusions on endothelial function in hospitalized patients. Transfusion 2015; 55: 782–90.
67. Tinmouth A, Fergusson D, Yee IC, Hébert PC. Clinical consequences of red cell storage in the critically ill. Transfusion 2006; 46: 2014–27.
68. Purdy FR, Tweeddale MG, Merrick PM. Association of mortality with age of blood transfused in septic ICU patients, 1997. Can J Anaesth 1997; 44: 1256–61.
69. Koch CG, Li L, Sessler DI, Figueroa P, Hoeltge GA, Mihaljevic T, Blackstone EH. Duration of red-cell storage and complications after cardiac surgery. N Engl J Med 2008; 358: 1229–39.
70. Sanders J, Patel S, Cooper J, Berryman J, Farrar D, Mythen M, Montgomery HE. Red blood cell storage is associated with length of stay and renal complications after cardiac surgery. Transfusion 2011; 51: 2286–94.
71. Janz DR, Zhao Z, Koyama T, May AK, Bernard GR, Bastarache JA, Young PP, Ware LB. Longer storage duration of red blood cells is associated with an increased risk of acute lung injury in patients with sepsis. Ann Intensive Care 2013; 3: 33.
72. Juffermans NP, Vlaar APJ, Prins DJ, Goslings JC, Binnekade JM. The age of red blood cells is associated with bacterial infections in critically ill trauma patients. Blood Transfus 2012; 10: 290–5.
73. van Straten AHM, Soliman Hamad MA, van Zundert AAJ, Martens EJ, ter Woorst JF, de Wolf AM, Scharnhorst V. Effect of duration of red blood cell storage on early and late mortality after coronary artery bypass grafting. J Thorac Cardiovasc Surg 2011; 141: 231–7.
74. Kor DJ, Kashyap R, Weiskopf RB, Wilson GA, van Buskirk CM, Winters JL, Malinchoc M, Hubmayr RD, Gajic O. Fresh red blood cell transfusion and short-term pulmonary, immunologic, and coagulation status: a randomized clinical trial. Am J Respir Crit Care Med 2012; 185: 842–50.
75. Aubron C, Bailey M, McQuilten Z, Pilcher D, Hegarty C, Martinelli A, Magrin G, Irving D, Cooper DJ, Bellomo R. Duration of red blood cells storage and outcome in critically ill patients. J Crit Care 2014; 29: 476.e1–8.
76. Goel R, Johnson DJ, Scott AV, Tobian AAR, Ness PM, Nagababu E, Frank SM. Red blood cells stored 35 days or more are associated with adverse outcomes in high-risk patients. Transfusion 2016; 56: 1690–8.
77. Martí-Carvajal Arturo J, Simancas-Racines D, Peña-González Barbra S. Prolonged storage of packed red blood cells for blood transfusion. Cochrane Database Syst Rev 2015; https://doi.org/10.1002/14651858.CD009330.
78. Halmin M, Rostgaard K, Lee BK, Wikman A, Norda R, Nielsen KR, Pedersen OB, Holmqvist J, Hjalgrim H, Edgren G. Length of storage of red blood cells and patient survival after blood transfusion. Ann Intern Med 2017; 166: 248–56.
79. Lacroix J, Hebert PC, Fergusson D, Tinmouth A, Cook DJ, Marshall JC, Clayton L, Sc M, Mcintyre L, Callum J, Turgeon AF, Blajchman MA, Walsh TS, Stanworth SJ, Campbell H, Phil D, Capellier G, Tiberghien P, Bardiaux L, Van De Watering L, Van Der Meer NJ, Sabri E, Sc M, Vo D, Eng B. Age of transfused blood in critically ill adults. N Engl J Med 2015; 372: 1410–8.
80. Heddle NM, Cook RJ, Arnold DM, Liu Y, Barty R, Crowther MA, Devereaux PJ, Hirsh J, Warkentin TE, Webert KE, Roxby D, Sobieraj-Teague M, Kurz A, Sessler DI, Figueroa P, Ellis M, Eikelboom JW. Effect of short-term vs. long-term blood storage on mortality after transfusion. N Engl J Med 2016; 375: 1937–45.
81. Higgins JPT, Green S (editors). Cochrane handbook for systematic reviews of interventions version 5.1.0. The Cochrane Collaboration, 2011. Available from http://handbook.cochrane.org [updated March 2011].
82. Liberati A, Altman DG, Tetzlaff J, Mulrow C, Gøtzsche PC, Ioannidis JPA, Clarke M, Devereaux PJ, Kleijnen J, Moher D. The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate health care interventions: explanation and elaboration. PLoS Med 2009; 6: e1000100.
83. Shamseer L, Moher D, Clarke M, Ghersi D, Liberati A, Petticrew M, Shekelle P, Stewart LA, PRISMA-P Group. Preferred reporting items for systematic review and meta-analysis protocols (PRISMA-P) 2015: elaboration and explanation. BMJ 2015; 349: g7647.
84. International conference on harmonisation of technical requirements for registration of pharmaceuticals for human use. Integrated Addendum To ICH E6 (R1): Guideline for Good Clinical Practice, 2015; 2.
85. Higgins JPT, Altman DG, Gotzsche PC, Juni P, Moher D, Oxman AD, Savovic J, Schulz KF, Weeks L, Sterne JAC. The Cochrane Collaboration's tool for assessing risk of bias in randomised trials. BMJ 2011; 343: d5928.
86. Jakobsen JC, Wetterslev J, Winkel P, Lange T, Gluud C. Thresholds for statistical and clinical significance in systematic reviews with meta-analytic methods. BMC Med Res Methodol 2014; 14: 120.
87. Harbord RM, Egger M, Sterne JAC. A modified test for small-study effects in meta-analyses of controlled trials with binary endpoints. Stat Med 2006; 25: 3443–57.
88. Egger M, Davey Smith G, Schneider M, Minder C. Bias in meta-analysis detected by a simple, graphical test. Br Med J 1997; 315: 629–34.
89. Begg CB, Mazumdar M. Operating characteristics of a rank correlation test for publication bias. Biometrics 1994; 50: 1088–101.
90. Atkins D, Best D, Briss PA, Eccles M, Falck-Ytter Y, Flottorp S, Guyatt GH, Harbour RT, Haugh MC, Henry D, Hill S, Jaeschke R, Leng G, Liberati A, Magrini N, Mason J, Middleton P, Mrukowicz J, O'Connell D, Oxman AD, Phillips B, Schünemann HJ, Edejer TT-T, Varonen H, Vist GE, Williams JW, Zaza S, GRADE Working Group. Grading quality of evidence and strength of recommendations. BMJ 2004; 328: 1490.
91. Deeks JHJ. Statistical algorithms in Review Manager 5. RevMan 53, 2010.
92. Dersimonian R, Laird N. Meta-analysis in clinical trials*. Stat Med 1986; 188: 177–88.
93. Mantel N, Haenszel W. Statistical aspects of the analysis of data from retrospective studies of disease. J Natl Cancer Inst 1959; 22: 719–48.
94. Demets D. Methods for combining randomized clinical trials: strengths and limitations. Stat Med 1987; 6: 341–50.
95. Higgins JPT, Spiegelhalter DJ. Being sceptical about meta-analyses: a Bayesian perspective on magnesium trials in myocardial infarction. Int J Epidemiol 2002; 31: 96–104.
96. The Magnesium in Coronaries. (MAGIC) Trial I. Early administration of intravenous magnesium to high-risk patients with acute myocardial infarction in the Magnesium in Coronaries (MAGIC) Trial: a randomised controlled trial. Lancet 2002; 360: 1189–96.
97. Woods K, Abrams K. The importance of effect mechanism in the design and interpretation of clinical trials: the role of magnesium in acute myocardial infarction. Prog Cardiovasc Dis 2002; 44: 267–74.
98. Jakobsen JC, Wetterslev J, Lange T, Gluud C. Viewpoint: taking into account risks of random errors when analysing multiple outcomes in systematic reviews. Cochrane Database Syst Rev 2016; 3: ED000111.
99. Brok J, Thorlund K, Gluud C, Wetterslev J. Trial sequential analysis reveals insufficient information size and potentially false positive results in many meta-analyses. J Clin Epidemiol 2008; 61: 763–9.
100. Brok J, Thorlund K, Wetterslev J, Gluud C. Apparently conclusive meta-analyses may be inconclusive – Trial sequential analysis adjustment of random error risk due to repetitive testing of accumulating data in apparently conclusive neonatal meta-analyses. Int J Epidemiol 2009; 38: 287–98.
101. Higgins JPT, Whitehead A, Simmonds M. Sequential methods for random-effects meta-analysis. Stat Med 2011; 30: 903–21.
102. Imberger G, Gluud C, Boylan J, Wetterslev J. Systematic reviews of anesthesiologic interventions reported as statistically significant: problems with power, precision, and type 1 error protection. Anesth Analg 2015; 121: 1611–22.
103. Mascha EJ. Alpha, beta, meta: guidelines for assessing power and Type I error in meta-analyses. Anesth Analg 2015; 121: 1430–3.
104. Pogue JM, Yusuf S. Cumulating evidence from randomized trials: utilizing sequential monitoring boundaries for cumulative meta-analysis. Control Clin Trials 1997; 18: 580–93.
105. Terkawi AS, Mavridis D, Flood P, Wetterslev J, Terkawi RS, Bin Abdulhak AA, Nunemaker MS, Tiouririne M. Does ondansetron modify sympathectomy due to subarachnoid anesthesia? Anesthesiology 2016; 124: 1.
106. Thorlund K, Devereaux PJ, Wetterslev J, Guyatt G, Ioannidis JPA, Thabane L, Gluud LL, Als-Nielsen B, Gluud C. Can trial sequential monitoring boundaries reduce spurious inferences from meta-analyses? Int J Epidemiol 2009; 38: 276–86.
107. Wetterslev J, Thorlund K, Brok J, Gluud C. Trial sequential analysis may establish when firm evidence is reached in cumulative meta-analysis. J Clin Epidemiol 2008; 61: 64–75.
108. TSA. Trial sequential analysis (TSA) (Computer program on www.ctu.dk/tsa/). Copenhagen Trial Unit 2011.
109. Gluud C, Thorlund K, Engstrøm J, Wetterslev J, Brok J, Imberger G. User manual for trial sequential analysis (TSA). Copenhagen Trial Unit 2016.
110. Kulinskaya E, Wood J. Trial sequential methods for meta-analysis. Res Synth Methods 2014; 5: 212–20.
111. Wetterslev J, Thorlund K, Brok J, Gluud C. Estimating required information size by quantifying diversity in random-effects model meta-analyses. BMC Med Res Methodol 2009; 9: 86.
112. Turner RM, Bird SM, Higgins JPT. The impact of study size on meta-analyses: examination of underpowered studies in cochrane reviews. PLoS ONE 2013; 8: 1–8.