Transfusion strategies for major haemorrhage in trauma
Corresponding Author
Nicola S. Curry
Oxford Haemophilia & Thrombosis Centre, Department of Haematology, Oxford University Hospitals NHS Trust, Churchill Hospital, Oxford, UK
NIHR BRC, Blood Theme, Oxford Centre for Haematology, Oxford, UK
Correspondence: Dr Nicola S. Curry, Oxford Haemophilia & Thrombosis Centre, Churchill Hospital, Headley Way, Oxford, OX3 7LE, UK.
E-mail: [email protected]
Search for more papers by this authorRoss Davenport
Centre for Trauma Sciences, Blizard Institute, Barts and the London School of Medicine & Dentistry, Queen Mary University of London, London, UK
Search for more papers by this authorCorresponding Author
Nicola S. Curry
Oxford Haemophilia & Thrombosis Centre, Department of Haematology, Oxford University Hospitals NHS Trust, Churchill Hospital, Oxford, UK
NIHR BRC, Blood Theme, Oxford Centre for Haematology, Oxford, UK
Correspondence: Dr Nicola S. Curry, Oxford Haemophilia & Thrombosis Centre, Churchill Hospital, Headley Way, Oxford, OX3 7LE, UK.
E-mail: [email protected]
Search for more papers by this authorRoss Davenport
Centre for Trauma Sciences, Blizard Institute, Barts and the London School of Medicine & Dentistry, Queen Mary University of London, London, UK
Search for more papers by this authorSummary
Trauma is a leading cause of death worldwide in persons under 44 years of age, and uncontrolled haemorrhage is the most common preventable cause of death in this patient group. The transfusion management of trauma haemorrhage is unrecognisable from 20 years ago. Changes in clinical practice have been driven primarily by an increased understanding of the pathophysiology of trauma-induced coagulopathy (TIC), which is associated with poor clinical outcomes, including a 3- to 4-fold increased risk of death. Targeting this coagulopathy alongside changes to surgical and anaesthetic practices (an overarching strategy known as damage control surgery/damage control resuscitation) has led to a significant reduction in mortality rates over the last two decades. This narrative review will discuss the transfusion practices that are currently used for trauma haemorrhage and the evidence that supports these practices.
References
- Bakaas-Aasen, K., Van Dieren, S., Balvers, K., Juffermans, N.P., Noess, P.A., Rourke, C., Eaglestone, S., Ostrowski, S.R., Stensballe, J., Stanworth, S., Maegele, M., Goslings, C., Johansson, P.I., Brohi, K. & Gaarder, C.; the TACTIC/INTRN collaborators. (2018) Data-driven development of ROTEM and TEG algorithms for the management of trauma haemorrhage. A prospective observational multicentre study. Annals of Surgery, [e-pub, ahead of print] https://doi.org/10.1097/sla.0000000000002825
10.1097/SLA.0000000000002825 Google Scholar
- Boffard, K.D., Riou, B., Warren, B., Choong, P.I., Rizoli, S., Rossaint, R., Axelsen, M. & Kluger, Y.; NovoSeven Trauma Study Group. (2005) Recombinant factor VIIa as adjunctive therapy for bleeding control in severely injured trauma patients: two parallel randomized, placebo-controlled, double-blind clinical trials. Journal of Trauma, 59, 8–18.
- Bolliger, D., Görlinger, K. & Tanaka, K.A. (2010) Pathophysiology and treatment of coagulopathy in massive hemorrhage and hemodilution. Anesthesiology, 113, 1205–1219.
- Booth, C. & Allard, S. (2018) Major haemorrhage protocols. ISBT Science Series, 13, 219–228.
10.1111/voxs.12428 Google Scholar
- Brohi, K., Singh, J., Heron, M. & Coats, T. (2003) Acute traumatic coagulopathy. Journal of Trauma, 54, 1127–1130.
- Brohi, K., Cohen, M.J., Ganter, M.T., Schultz, M.J., Levi, M., Mackenersie, R.C. & Pittet, J.F. (2008) Acute traumatic coagulopathy of trauma: hypoperfusion induces systemic anticoagulation and hyperfibrinolysis. Journal of Trauma, 64, 1211–1217.
- Campbell, H.E., Stokes, E.A., Bargo, D.N., Curry, N., Lecky, F.E., Edwards, A., Woodford, M., Seeney, F., Eaglestone, S., Brohi, K., Gray, A.M. & Stanworth, S.J. (2015) Quantifying the healthcare costs of treating severely bleeding major trauma patients: a national study for England. Critical Care, 19, 276.
- Cap, A.P. & Hunt, B. (2014) Acute traumatic coagulopathy. Current Opinion in Critical Care, 20, 638–645.
- Cap, A.P. & Perkins, J.G. (2011) Lyophilized platelets: challenges and opportunities. Journal of Trauma, 7 (5 Suppl), S59–S60.
10.1097/TA.0b013e31821a606d Google Scholar
- Cap, A.P., Beckett, A., Benov, A., Borgman, M., Chen, J., Corley, J.B., Doughty, H., Fisher, A., Glasberg, E., Gonzales, R., Kane, S.F., Malloy, W.W., Nessen, S., Perkins, J.G., Prat, N., Quesada, J., Reade, M., Sailliol, A., Spinella, P.C., Stockinger, Z., Strandenes, G., Taylor, A., Yazer, M., Bryant, B. & Gurney, J. (2018) Whole blood transfusion. Military Medicine, 183, 44–51.
- Cardenas, J.C., Rahbar, E., Pommerening, M.J., Baer, L.A., Matijevic, N., Cotton, B.A., Holcomb, J.B. & Wade, C.E. (2014) Measuring thrombin generation as a tool for predicting haemostatic potential and transfusion requirements following trauma. Journal of Trauma and Acute Care Surgery, 7, 839–845.
- Centers for Disease Control and Prevention, National Center for Injury Prevention and Control. Web-based Injury Statistics Query and Reporting System (WISQARS) Fatal Injury Data. (2017). Available at: https://www.cdc.gov/injury/wisqars/fatal.html (accessed 13 October 2018).
- Chapman, M.P., Moore, E.E., Moore, H.B., Gonzalez, E., Gamboni, F., Chandler, J.G., Mitra, S., Ghasabyan, A., Chin, T.L., Sauaia, A., Banerjee, A. & Silliman, C.C. (2016) Overwhelming tPA release, not PAI-1 degradation, is responsible for hyperfibrinolysis in severely injured trauma patients. Journal of Trauma and Acute Care Surgery, 80, 16–23.
- Cohen, M.J., Kutcher, M., Redick, B., Nelson, M., Call, M., Knudson, M.M., Schreiber, M.A., Bulger, E.M., Muskat, P., Alarcon, L.H., Myers, J.G., Rahbar, M.H., Brasel, K.J., Phelan, H.A., del Junco, D.J., Fox, E.E., Wade, C.E., Holcomb, J.B., Cotton, B.A. & Matijevic, N.; PROMMTT Study Group. (2013) Clinical and mechanistic drivers of acute traumatic coagulopathy. Journal of Trauma and Acute Care Surgery, 75 (Suppl), S40–S47.
- Cotton, B.A., Gunter, O.L., Isbell, J., Au, B.K., Robertson, A.M., Morris, J.A. Jr, St Jaques, P. & Young, P.P. (2008) Damage control hematology: the impact of a trauma exsanguination protocol on survival and blood product utilization. Journal of Trauma, 64, 1177–1182.
- Cotton, B.A., Reddy, N., Hatch, Q.M., LeFebyre, E., Wade, C.E., Kozar, R.A., Gill, B.S., Albarado, R., McNutt, M.K. & Holcomb, J.B. (2011a) Damage control resuscitation is associated with a reduction in resuscitation volumes and improvement in survival in 390 damage control laparotomy patients. Annals of Surgery, 254, 598–605.
- Cotton, B.A., Faz, G., Hatch, Q.M., Radwan, Z.A., Podbielski, J., Wade, C., Kozar, R.A. & Holcomb, J.B. (2011b) Rapid thrombelastography delivers real-time results that predict transfusion within 1 hour of admission. Journal of Trauma, 71, 407–417.
- Cotton, B.A., Podbielski, J., Camp, E., Welch, T., del Junco, D., Bai, Y., Hobbs, R., Scroggins, J., Hartwell, B., Kozar, R.A., Wade, C.E. & Holcomb, J.B. (2013) A randomized controlled pilot trial of modified whole blood versus component therapy in severely injured patients requiring large volume transfusions. Annals of Surgery, 258, 527–532.
- CRASH-2 trial collaborators. (2010) Effects of tranexamic acid on death, vascular occlusive events, and blood transfusion in trauma patients with significant haemorrhage (CRASH-2): a randomised, placebo-controlled trial. Lancet, 376, 23–32.
- CRASH-2 trial collaborators. (2011) The importance if early treatment with tranexamic acid in bleeding trauma patients: an exploratory analysis of the CRASH-2 randomised controlled trial. Lancet, 377, 1096–1101.
- Curry, N.S., Hopewell, S., Doree, C., Hyde, C., Brohi, K. & Stanworth, S. (2011) The acute management of trauma hemorrhage: a systematic review of randomized controlled trials. Critical Care, 15, R92.
- Curry, N., Rourke, C., Davenport, R., Beer, S., Pankhurst, L., Deary, A., Thomas, H., Llewelyn, C., Green, L., Doughty, H., Nordmann, G., Brohi, K. & Stanworth, S. (2015) Early cryoprecipitate for major haemorrhage in trauma: a randomised controlled feasibility trial. British Journal of Anaesthesia, 115, 76–83.
- Curry, N.S., Davenport, R., Pavord, S., Mallett, S.V., Kitchen, D., Klein, A.A., Maybury, H., Collins, P.W. & Laffan, M. (2018a) The use of viscoelastic haemostatic guidelines in the management of major bleeding: a British Society for Haematology Guideline. British Journal of Haematology, 182, 789–806.
- Curry, N., Foley, C., Wong, H., Mora, A., Curnow, E., Zarankaite, A., Hodge, R., Hopkins, V., Deary, A., Ray, J., Moss, P., Reed, M.J., Kellett, S., Davenport, R. & Stanworth, S. (2018b) Early fibrinogen concentrate therapy for major haemorrhage in trauma (E-FIT-1): results from a UK multi-centre, randomised, double blind, placebo-controlled pilot trial. Critical Care, 18, 164.
- Daniel, Y., Habas, S., Malan, L., Escarment, J., David, J.S. & Peyrefitte, S. (2016) Tactical damage control resuscitation in austere military environments. Journal Royal Army Medical Corps, 162, 419–427.
- Davenport, R.A. & Brohi, K. (2016) Cause of trauma-induced coagulopathy. Current Opinion in Anaesthesiology, 29, 212–219.
- Davenport, R., Manson, J., De'Ath, H., Platton, S., Coates, A., Allard, S., Hart, D., Pearse, R., Pasi, K.J., MacCallum, P., Stanworth, S. & Brohi, K. (2011) Functional definition and characterization of acute traumatic coagulopathy. Critical Care Medicine, 39, 2652–2658.
- Davenport, R.A., Guerreiro, M., Rourke, C., Platton, S., Cohen, M., Pearse, R., Thiemermann, C. & Brohi, K. (2017) Activated protein C drives the hyperfibrinolysis of acute traumatic coagulopathy. Anesthesiology, 126, 115–127.
- Dumont, L.J., Slichter, S.J. & Reade, M.C. (2014) Cryopreserved platelets: frozen in a logjam? Transfusion, 54, 1907–1910.
- Dunbar, N.M. & Chandler, W.L. (2009) Thrombin generation in trauma patients. Transfusion, 49, 2652–2660.
- Frith, D., Goslings, J.C., Gaarder, C., Maegele, M., Cohen, M.J., Allard, S., Johansson, P.I., Stanworth, S., Thiemermann, C. & Brohi, K. (2010) Definition and drivers of acute traumatic coagulopathy: clinical and experimental investigations. Journal of Thrombosis and Haemostasis, 8, 1919–1925.
- Gall, L.S., Vulliamy, P., Gillespie, S., Jones, T.F., Pierre, R.S.J., Breukers, S.E., Gaarder, C., Juffermans, N.P., Maegele, M., Stensballe, J., Johansson, P.I., Davenport, R.A. & Brohi, K.; Targeted Action for Curing Trauma-Induced Coagulopathy (TACTIC) partners. (2018) The S100A10 pathway mediates an occult hyperfibrinolytic subtype in trauma patients. Annals of Surgery. https://doi.org/10.1097/SLA.0000000000002733
10.1097/SLA.0000000000002733 Google Scholar
- Garrigue, D., Godier, A., Glacet, A., Labreuche, J., Kipnis, E., Paris, C., Duhamel, A., Resch, A., Bauters, A., Machuron, F., Renom, P., Goldstein, P., Tavernier, B., Sailliol, A. & Susen, S. (2017) French lyophilised plasma versus fresh frozen plasma for the initial management of trauma-induced coagulopathy: a randomized open-label trial. Journal of Thrombosis and Haemostasis, 16, 481–489.
- Gayet-Ageron, A., Prieto-Merino, D., Ker, K., Shakur, H., Ageron, F.X., Roberts, I. & Collaboration, Antifibrinolytics Trials (2018) Effect of treatment delay on the effectiveness and safety of antifibrinolytics in acute severe haemorrhage: a meta-analysis of individual patient-level data from 40 138 bleeding patients. Lancet, 3910, 125–132.
- Gilstad, C., Roschewski, M., Wells, J., Delmas, A., Lackey, J., Uribe, P., Popa, C., Jardeleza, T. & Roop, S. (2012) Fatal transfusion-associated graft-versus-host disease with concomitant immune hemolysis in a group A combat trauma patient resuscitated with group O fresh whole blood. Transfusion, 52, 930–935.
- Gonzalez, E., Moore, E.E., Moore, H.B., Chapman, M.P., Chin, T.L., Ghasabyan, A., Wohlauer, M.V., Barnett, C.C., Bensard, D.D., Biffl, W.L., Burlew, C.C., Johnson, J.L., Pieracci, F.M., Jurkovich, G.J., Banerjee, A., Silliman, C.C. & Sauaia, A. (2016) Goal-directed hemostatic resuscitation of trauma-induced coagulopathy a pragmatic randomized clinical trial comparing a viscoelastic assay to conventional coagulation assays. Annals of Surgery, 263, 1051–1059.
- Green, L., Backholer, L., Wiltshire, M., Platton, S., Stanworth, S.J. & Cardigan, R. (2016) The hemostatic properties of thawed pooled cryoprecipitate up to 72 hours. Transfusion, 56, 1356–1361.
- Griggs, J.E., Jeyanathan, J., Joy, M., Russell, M.Q., Durge, N., Bootland, D., Dunn, S., Sausmarez, E.D., Wareham, G., Weaver, A. & Lyon, R.M.; on behalf of Kent, Surrey & Sussex Air Ambulance Trust. (2018) Mortality of civilian patients with suspected traumatic haemorrhage receiving pre-hospital transfusion of packed red blood cells compared to pre-hospital crystalloid. Scandinavian Journal of Trauma, Resuscitation and Emergency Medicine, 26, 100.
- Grottke, O., Braunschweig, T., Spronk, H.M., Esch, S., Rieg, A.D., van Oerle, R., ten Cate, H., Tolba, R. & Rossaint, R. (2011) Increasing concentrations of prothrombin complex concentrate induce DIC in a pig model of coagulopathy with blunt liver injury. Blood, 118, 1943–1951.
- Hagemo, J.S., Christiaans, S.C., Stanworth, S.J., Brohi, K., Johansson, P.I., Goslings, J.C., Naess, P.A. & Gaarder, C. (2015) Detection of acute traumatic coagulopathy and massive transfusion requirements by means of rotational thromboelastometry: an international prospective validation study. Critical Care, 19, 97.
- Hallet, J., Lauzier, F., Mailloux, O., Trottier, V., Archambault, P., Zarychanski, R. & Turgeon, A.F. (2013) The use of higher platelet: RBC transfusion ratio in the acute phase of trauma resuscitation: a systematic review. Critical Care Medicine, 41, 2800–2811.
- Hauser, C.J., Boffard, K., Dutton, R., Bernard, G.R., Croce, M.A., Holcomb, J.B., Leppaniemi, A., Parr, M., Vincent, J.L., Tortella, B.J., Dimsits, J. & Bouillon, B.; CONTROL Study Group. (2010) Results of the CONTROL trial: efficacy and safety of recombinant activated Factor VII in the management of refractory traumatic hemorrhage. Journal of Trauma, 69, 489–500.
- Hiippala, S.T., Myllylä, G.J. & Vahtera, E.M. (1995) Hemostatic factors and replacement of major blood loss with plasma-poor red cell concentrates. Anesthesia and Analgesia, 81, 360–365.
- Holcomb, J., del Junco, D.J., Fox, E.E., Wade, C.E., Cohen, M.J., Schreiber, M.A., Alarcon, L.H., Bai, Y., Brasel, K.J., Bulger, E.M., Cotton, B.A., Matijevic, N., Muskat, P., Myers, J.G., Phelan, H.A., White, C.E., Zhang, J. & Rahbar, M.H.; PROMMTT Study Group. (2013) The prospective, observational, multicenter, major trauma transfusion (PROMMTT) study: comparative effectiveness of a time-varying treatment with competing risks. Journal of the American Medical Association Surgery, 148, 127–136.
- Holcomb, J., Tilley, B.C., Baraniuk, S., Fox, E.E., Wade, C.E., Podbileski, J.M., del Junco, D.J., Brasel, K.J., Bulger, E.M., Callcut, R.A., Cohen, M.J., Cotton, B.A., Fabian, T.C., Inaba, K., Kerby, J.D., Muskat, P., O'Keeffe, T., Rizoli, S., Robinson, B.R., Scalea, T.M., Schreiber, M.A., Stein, D.M., Weinberg, J.A., Callum, J.L., Hess, J.R., Matijevic, N., Miller, C.N., Pittet, J.F., Hoyt, D.B., Pearson, G.D., Leroux, B. & van Belle, G.; PROPPR Study Group. (2015) Transfusion of plasma, platelets, and red blood cells in a 1:1:1 vs a 1:1:2 ratio and mortality in patients with severe trauma. The PROPPR randomized clinical trial. Journal of the American Medical Association, 313, 471–482.
- Hunt, B.J., Allard, S., Keeling, D., Norfolk, D., Stanworth, S.J. & Pendry, K.; on behalf of the BCSH. (2015) A practical guideline for the haematological management of major haemorrhage. British Journal of Haematology, 170, 788–803.
- Inaba, K., Lustenberger, T., Rhee, P., Holcomb, J.B., Blackbourne, L.H., Shulman, I., Nelson, J., Talving, P. & Demetriades, D. (2010) The impact of platelet transfusion in massively transfused trauma patients. Journal of the American College of Surgeons, 211, 573–579.
- Inaba, K., Barmparas, G., Rhee, P., Branco, B.C., Fitzpatrick, M., Okoye, O.T. & Demetriades, D. (2014) Dried platelets in a swine model of liver injury. Shock, 41, 429–434.
- Innerhofer, P., Fries, D., Mittermayr, M., Innerhofer, N., von Langen, D., Hell, T., Gruber, G., Schmid, S., Friesenecker, B., Lorenz, I.H., Strohle, M., Rastner, V., Trubsbach, S., Raab, H., Treml, B., Wally, D., Treichl, B., Mayr, A., Kranewitter, C. & Oswald, E. (2017) Reversal of trauma-induced coagulopathy using first-line coagulation factor concentrates or fresh frozen plasma (RETIC): a single-centre, parallel-group, open-label, randomised trial. Lancet Haematology, 4, e258–e271.
- Jehan, F., Aziz, H., O'Keefe, T., Khan, M., Zakaria, E.R., Hamidi, M., Zeeshan, M., Kulvatunyou, N. & Joseph, B. (2018) The role of four-factor prothrombin complex concentrate in coagulopathy of trauma: a propensity matched analysis. Journal of Trauma and Acute Care Surgery, 85, 18–24.
- Johansson, P.I., Stensballe, J., Rasmussen, L.S. & Ostrowski, S.R. (2011) A high admission syndecan-1 level, a marker of endothelial glycocalyx degradation, is associated with inflammation, protein C depletion, fibrinolysis, and increased mortality in trauma patients. Annals of Surgery, 254, 194–200.
- Johnson, L., Coorey, C.P. & Marks, D.C. (2014) The haemostatic activity of cryopreserved platelets is mediated by phosphatidylserine-expressing platelets and platelet microparticles. Transfusion, 54, 1917–1926.
- del Junco, D.J., Holcomb, J.B., Fox, E.E., Brasel, K.J., Phelan, H.A., Bulger, E.M., Schreiber, M.A., Muskat, P., Alarcon, L.H., Cohen, M.J., Cotton, B.A., Wade, C.E., Myers, J.G. & Rahbar, M.H.; on behalf of the PROMMTT Study Group. (2013) Resuscitate early with plasma and platelets or balance blood products gradually: findings from the prospective, observational, multicenter, major trauma transfusion (PROMMTT) study. Journal of Trauma and Acute Care Surgery, 75 (Suppl) , S24–S30.
- Khan, S., Davenport, R., Raza, I., Glasgow, S., De'Ath, H.D., Johansoon, P.I., Curry, N., Stanworth, S., Gaarder, C. & Brohi, K. (2015) Damage control resuscitation using blood component therapy in standard doses has a limited effect on coagulopathy during trauma haemorrhage. Intensive Care Medicine, 41, 239–247.
- Kozar, R.A., Peng, Z., Zhang, R., Holcomb, J.B., Pati, S., Park, P., Ko, T.C. & Paredes, A. (2011) Plasma restoration of endothelial glycocalyx in a rodent model of hemorrhagic shock. Anesthesia and Analgesia, 112, 1289–1295.
- Kutcher, M.E., Redick, B.J., McCreery, R.C., Crane, I.M., Greenberg, M.D., Cachola, L.M., Nelson, M.F. & Cohen, M.J. (2012) Characterization of platelet dysfunction after trauma. Journal of Trauma and Acute Care Surgery, 73, 13–19.
- Lelkens, C.C., Koning, J.G., de Kort, B., Floot, I.B. & Noorman, F. (2006) Experiences with frozen blood products in the Netherlands military. Transfusion Apheresis Science, 34, 289–298.
- Lord, J.M., Midwinter, M.J., Chen, Y.-F., Belli, A., Brohi, K., Kovacs, E.J., Koenderman, L., Kubes, P. & Lilford, R.J. (2014) The systemic immune response to trauma: an overview of pathophysiology and treatment. Lancet, 384, 1455–1465.
- MacLeod, J.B., Lynn, M., McKenny, M.G., Cohn, S.M. & Murtha, M. (2003) Early coagulopathy predicts mortality in trauma. Journal of Trauma, 55, 39–44.
- Maegele, M., Lefering, R., Yucel, N., Tjardes, T., Rixen, D., Paffrath, T., Simanski, C., Neugebauer, E. & Bouillon, B.; AG Polytrauma of the German Trauma Society (DGU). (2007) Early coagulopathy in multiple injury: an analysis from the German Trauma Registry on 8724 patients. Injury, 38, 298–304.
- Marks, D. (2018) Cryopreserved platelets: are we there yet? Transfusion, 58, 2092–2094.
- Marsden, M., Benger, J., Brohi, K., Curry, N., Foley, C., Green, L., Lucas, J., Rossetto, A., Stanworth, S., Thomas, H. & Davenport, R.; on behalf of the CRYOSTAT-2 investigators. (2018) Coagulopathy, cryoprecipitate and CRYOSTAT-2: realising the potential of a nationwide trauma system for a national clinical trial. British Journal of Anaesthesia. https://doi.org/10.1016/j.bja.2018.10.055
- Meyer, A.S., Meyer, M.A.S., Sorensen, A.M., Rasmussen, L.S., Hansen, M.B., Holcomb, J.B., Cotton, B.A.C., Wade, C.E., Ostrowski, S.R. & Johansson, P.I. (2014) Thrombelastography and rotational thromboelastometry early amplitudes in 182 trauma patients with clinical suspicion of severe injury. Journal of Trauma and Acute Care Surgery, 76, 682–690.
- Moore, H.B., Moore, E.E., Chapman, M.P., Gonzalez, E., Slaughter, A.L., Morton, A.P., D'Alessandro, A., Hansen, K.C., Sauaia, A., Banerjee, A. & Silliman, C.C. (2015) Viscoelastic measurements of platelet function, not fibrinogen function, predicts sensitivity to tissue-type plasminogen activator in trauma patients. Journal of Thrombosis and Haemostasis, 13, 1878–1887.
- Moore, H.B., Moore, E.E., Chapman, M.P., Huebner, B.R., Einersen, P.M., Oushy, S., Silliman, C.C., Banerjee, A. & Sauaia, A. (2017) Viscoelastic tissue plasminogen activator challenge predicts massive transfusion in 15 minutes. Journal of the American College of Surgeons, 225, 138–147.
- Moore, H.B., Moore, E.E., Chapman, M.P., McVaney, K., Bryskiewicz, G., Blechar, R., Chin, T., Burlew, C.C., Pieracci, F., West, F.B., Fleming, C.D., Ghasabayan, A., Chandler, J., Silliman, C.C., Banerjee, A. & Sauaia, A. (2018) Plasma-first resuscitation to treat haemorrhagic shock during emergency ground transportation in an urban area: a randomised trial. Lancet, 392, 283–291.
- Murad, M.H., Stubbs, J.R., Gandhi, M.J., Wang, A.T., Paul, A., Erwin, P.J., Montori, V.M. & Roback, J.D. (2010) The effect of plasma transfusion on morbidity and mortality: a systematic review and meta-analysis. Transfusion, 50, 1370–1383.
- Nair, P.M., Pidcoke, H.F., Cap, A.P. & Ramasubramanian, A.K. (2014) Effect of cold storage on shear induced platelet aggregation and clot strength. Journal of Trauma and Acute Care Surgery, 77, S88–S93.
- Nascimento, B., Callum, J., Tien, H., Rubenfeld, G., Pinto, R., Lin, Y. & Rizoli, S. (2013) Effect of a fixed-ratio (1:1:1) transfusion protocol versus laboratory-results-guided transfusion in patients with severe trauma: a randomized feasibility trial. Canadian Medical Association Journal, 185, E583–E589.
- Nascimento, B., Callum, J., Tien, H., Peng, H., Rizoli, S., Karanicolas, P., Alam, A., Xiong, W., Selby, R., Garzon, A.-M., Colavecchia, C., Howald, R., Nathens, A. & Beckett, A. (2016) Fibrinogen in the initial resuscitation of severe trauma (FiiRST): a randomized feasibility trial. British Journal of Anaesthesia, 117, 775–782.
- National Clinical Guideline Centre. (2016) Major trauma: assessment and initial management. NICE Guideline NG39 ©2016 National Clinical Guideline Centre. Available at: www.nice.org.uk/guidance/ng39/evidence/full-guideline-2308122833 Pages 236-239 (accessed 14 October 2018)
- Naumann, D.N., Khan, M.A., Smith, J.E., Rickard, R. & Wooley, T. (2018) Future strategies for remote damage control resuscitation after traumatic haemorrhage. Journal of Trauma. https://doi.org/10.1097/TA.0000000000002080)
- Nessen, S.C., Eastridge, B.J., Cronk, D., Craig, R.M., Berseus, O., Ellison, R., Remick, K., Seery, J., Shah, A. & Spinella, P.C. (2013) Fresh whole blood use by forward surgical teams in Afghanistan is associated with improved survival compared to component therapy without platelets. Transfusion, 53 (Suppl 1), 107S–113S.
- Nienaber, U., Innerhofer, P., Westermann, I., Schöchl, H., Attal, R., Breitkopf, R. & Maegele, M. (2011) The impact of fresh frozen plasma vs. coagulation factor concentrates on morbidity and mortality in trauma-associated haemorrhage and massive transfusion. Injury, 42, 697–701.
- Noorman, F., van Dongen, T.T., Plat, M.J., Badloe, J.F., Hess, J.R. & Hoencamp, R. (2016) Transfusion: -80 degrees C frozen blood products are safe and effective in military casualty care. Public Library of Science One, 11, e0168401.
- Perkins, J.G., Cap, A.P., Spinella, P.C., Blackbourne, L.H., Grathwohl, K.W., Repine, T.B., Ketchum, L., Waterman, P., Lee, R.E., Beekley, A.C., Sebesta, J.A., Shorr, A.F., Wade, C.E. & Holcomb, J.B. (2009) An evaluation of the impact of apheresis platelets used in the setting of massively transfused trauma patients. Journal of Trauma, 66, S77–S84.
- Pidcoke, H.F., Spinella, P.C., Ramasubramanian, A.K., Strandenes, G., Hervig, T., Ness, P.M. & Cap, A.P. (2014) Refrigerated platelets for the treatment of acute bleeding: a review of the literature and re-examination of current standards. Shock, 41 (Suppl), S51–S53.
- Pohlman, T.H., Fecher, A.M. & Arreola-Garcia, C. (2018) Optimizing transfusion strategies in damage control resuscitation: current insights. Journal of Blood Medicine, 9, 117–133.
- Pusateri, A.E., Given, M.B., Schreiber, M.A., Spinella, P.C., Pati, S., Kozar, R.A., Khan, A., Dacorta, J.A., Kupferer, K.R., Prat, N., Pidcoke, H.F., Macdonald, V.W., Malloy, W.W., Sailliol, A. & Cap, A.P. (2016) Dried plasma: state of the science and recent developments. Transfusion, 56 (Suppl), S128–S139.
- Raynel, S., Padula, M.P., Marks, D.C. & Johnson, L. (2015) Cryopreservation alters the membrane and cytoskeletal protein profile of platelet microparticles. Transfusion, 55, 2422–2432.
- Raza, I., Davenport, R., Rourke, C., Platton, S., Manson, J., Spoors, C., Khan, S., De'Ath, H.D., Allard, S., Hart, D.P., Pasi, K.J., Hunt, B.J., Stanworth, S., MacCallum, P.K. & Brohi, K. (2013) The incidence and magnitude of fibrinolytic activation in trauma patients. Journal of Thrombosis and Haemostasis, 11, 307–314.
- Reddoch, K.M., Pidcoke, H.F., Montgomery, R.K., Fedyk, C.G., Aden, J.K., Ramasubramanian, A.K. & Cap, A.P. (2014) Hemostatic function of apheresis platelets stored at 4°C and 22°C. Shock, 41 (Suppl), S54–S61.
- Rehn, M., Weaver, A., Brohi, K., Eshelby, S., Green, L., Roislien, J. & Lockey, D.J. (2018) Effect of pre-hospital red blood cell transfusion on mortality and time of detah in civilian trauma patients. Shock. https://doi.org/10.1097/SHK.0000000000001166
- Rossaint, R., Bouillon, B., Cerny, V., Coats, T.J., Duranteau, J., Fernandez-Mondejar, E., Filipescu, D., Hunt, B.J., Komadina, R., Nardi, G., Neugebauer, E.A.M., Ozier, Y., Riddez, L., Schultz, A., Vincent, J-L. & Spahn, D.R. (2016) The European guideline on management of major bleeding and coagulopathy following trauma: fourth edition. Critical Care, 20, 100.
- Rourke, C., Curry, N., Khan, S., Taylor, R., Raza, I., Davenport, R., Stanworth, S. & Brohi, K. (2012) Fibrinogen levels during trauma hemorrhage, response to replacement therapy, and association with patient outcomes. Journal of Thrombosis and Haemostasis, 10, 1342–1351.
- Schafer, N., Driessen, A., Frohlich, M., Sturmer, E.K., Maegele, M.; TACTIC partners. (2015) Diversity in clinical management and protocols for the treatment of major bleeding trauma patients across European level 1 Trauma Centres. Scandinavian Journal of Trauma, Resuscitation and Emergency Medicine, 23, 74.
- Schöchl, H., Cotton, B., Inaba, K., Nienaber, U., Fischer, H., Voelckel, W. & Solomon, C. (2011a) FIBTEM provides early prediction of massive transfusion in trauma. Critical Care, 15, R265.
- Schöchl, H., Nienaber, U., Maegele, M., Hochleitner, G., Primavesi, G., Steitz, B., Arndt, C., Hanke, A., Voelckel, W. & Solomon, C. (2011b) Transfusion in trauma: thromboelastometry-guided coagulation factor concentrate-based therapy versus standard fresh frozen plasma-based therapy. Critical Care, 15, R83.
- Seheult, J.N., Bahr, M., Anto, V., Alarcon, L.H., Corcos, A., Sperry, J.L., Triulzi, D.J. & Yazer, M.H. (2018) safety profile of uncrossmatched, cold-stored, low-iter, group O+ whole blood in civilian trauma patients. Transfusion, 58, 2280–2288.
- Shaz, B.H., Dente, C.J., Nicholas, J., MacLeod, J.B., Young, A.N., Easley, K., Ling, Q., Harris, R.S. & Hillyer, C.D. (2010) Increased number of coagulation products in relationship to red blood cell products transfused improves mortality in trauma patients. Transfusion, 50, 493–500.
- Sheffield, W.P., Bhakta, V. & Jenkins, C. (2016) Stability of coagulation protein activities in single units or pools of cryoprecipitate during storage at 20-24°C for up to 24 h. Vox Sanguinis, 110, 12–19.
- Shlaifer, A., Siman-Tov, M., Radomislensky, I., Peleg, K., Shina, A., Baruch, E.N., Glassberg, E. & Yitzhak, A. (2017) Prehospital administration of freeze-dried plasma, is it the solution for trauma casualties? Journal of Trauma and Acute Care Surgery, 83, 675–682.
- Siletz, A., Burruss, S., Gruber, T., Ziman, A., Marder, V. & Cryer, H.M. (2017) Leukocyte filtration lesion impairs functional coagulation in banked whole blood. Journal of Trauma and Acute Care Surgery, 83, 420–426.
- Simpson, E., Lin, Y., Stanworth, S., Birchall, J., Doree, C. & Hyde, C. (2012) Recombinant factor VIIa for the prevention and treatment of bleeding in patients without haemophilia. Cochrane Database of Systematic Reviews, 14, CD005011.
- Solomon, C., Traintinger, S., Ziegler, B., Hanke, A., Rahe-Meyer, N., Voelckel, W. & Schochl, H. (2011) Platelet function following trauma. A multiplate electrode aggregometry study. Thrombosis Haemostasis, 106, 322–330.
- Sperry, J.L., Guyette, F.X., Brown, M.H., Yazer, M.H., Triulzi, D.J., Early-Young, B.J., Adams, P.W., Daley, B.J., Miller, R.S., Harbrecht, B.G., Claridge, J.A., Phelan, H.A., Witham, W.R., Putnam, A.T., Duane, T.M., Alarcon, L.H., Callaway, C.W., Zuckerbraun, B.S., Neal, M.D., Rosengart, M.R., Forsythe, R.M., Billiar, T.R., Peitzman, A.B. & Zenati, M.S.; for the PAMPer Study Group. (2018) Prehospital plasma during air medical transport in trauma patients at risk for haemorrhagic shock. New England Journal of Medicine, 379, 315–326.
- Spinella, P.C., Perkins, J.G., Grathwohl, K.W., Repine, T., Beekley, A.C., Sebesta, J., Jenkins, D., Azarow, K. & Holcomb, J.B. (2007) Risks associated with fresh whole blood and red blood cell transfusions in a combat support hospital. Critical Care Medicine, 35, 2576–2581.
- Strandenes, G., De Pasquale, M., Cap, A.P., Hervig, T.A., Kristoffersen, E.K., Hickey, M., Cordova, C., Berseus, O., Eliassen, H.S., Fisher, L., Williams, S. & Spinella, P.C. (2014) Emergency whole-blood use in the field: a simplified protocol for collection and transfusion. Shock, 41 (Suppl 1), 76–83.
- Strandenes, G., Austlid, I., Apelseth, T.O., Hervig, T.A., Sommerfelt-Pettersen, J., Herzig, M.C., Cap, A.P., Pidcoke, H.F. & Kristoffersen, E.K. (2015) Coagulation function of stored whole blood is preserved for 14 days in austere conditions: a ROTEM feasibility study during a Norwegian antipiracy mission and comparison to equal ratio reconstituted blood. Journal of Trauma and Acute Care Surgery, 78 (6 Suppl 1), S31–S38.
- Sunde, G.A., Vikenes, B., Strandenes, G., Flo, K.C., Hervig, T.A., Kristoffersen, E.K. & Heltne, J.K. (2015) Freeze dried plasma and fresh red blood cells for civilian prehospital hemorrhagic shock resuscitation. Journal of Trauma and Acute Care Surgery, 78 (6 Suppl 1), S26–S30.
- Vuillamy, P., Gillespie, S., Gall, L.S., Green, L., Brohi, K. & Davenport, R.A. (2017) Platelet transfusions reduce fibrinolysis but do not restore platelet function during trauma haemorrhage. Journal of Trauma and Acute Care Surgery, 83, 388–397.
- Watson, J.J., Pati, S. & Schreiber, M.A. (2016) Plasma transfusion: history, current realities, and novel improvements. Shock, 46, 468–479.
- Whiting, P., Al, M., Westwood, M., Corro Ramos, I., Ryder, S., Armstrong, N., Misso, K., Ross, J., Severens, J. & Kleijnen, J. (2015) Viscoelastic point-of-care testing to assist with the diagnosis, management and monitoring of haemostasis: a systematic review and cost-effectiveness analysis. Health Technology Assessment, 19 ISSN 1366-5278, 1–228. https://doi.org/10.3310/hta19580
- WOMAN Trial Collaborators. (2017) Effect of early tranexamic acid administration on mortality, hysterectomy, and other morbidities in women with post-partum haemorrhage (WOMAN): an international, randomised, double-blind, placebo-controlled trial. Lancet, 389, 2105–2116.
- Wong, H. & Curry, N. (2018) Do we need cryoprecipitate in the era of fibrinogen concentrate and other specific factor replacement options? Vox Sanguinis, 13, 23–28.
- Young, P.P., Cotton, B. & Goodnough, L.T. (2011) Massive transfusion protocols for patients with substantial haemorrhage. Transfusion Medicine Reviews, 25, 293–303.
- Zehtabchi, S. & Nishijima, D.K. (2009) Impact of transfusion of fresh-frozen plasma and packed red blood cells in a 1:1 ratio on survival of emergency department patients with severe trauma. Academic Emergency Medicine, 16, 371–378.