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Annals of Intensive Care

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Open Access 01-12-2011 | Research

The effect of red blood cell transfusion on tissue oxygenation and microcirculation in severe septic patients

Authors: Farid Sadaka, Ravi Aggu-Sher, Katie Krause, Jacklyn O'Brien, Eric S Armbrecht, Robert W Taylor

Published in: Annals of Intensive Care | Issue 1/2011

Abstract

Background

Microcirculation plays a vital role in the development of multiple organ failure in severe sepsis. The effects of red blood cell (RBC) transfusions on these tissue oxygenation and microcirculation variables in early severe sepsis are not well defined.

Methods

This is a prospective, observational study of patients with severe sepsis requiring RBC transfusions of one to two units of non-leukoreduced RBCs for a hemoglobin < 7.0, or for a hemoglobin between 7.0 and 9.0 with lactic acidosis or central venous oxygen saturation < 70%. This study took place in a 54-bed, medical-surgical intensive care unit of a university-affiliated hospital. Thenar tissue oxygen saturation was measured by using a tissue spectrometer on 21 patients, and a vaso-occlusive test was performed before and 1 hour after transfusion. The sublingual microcirculation was assessed with a Sidestream Dark Field device concomitantly on 11 of them.

Results

RBC transfusion resulted in increase in hemoglobin (7.23 (± 0.87) to 8.75 (± 1.06) g/dl; p < 0.001). RBC transfusion did not globally affect near-infrared spectrometry (NIRS)-derived variables. However, percent change in muscle oxygen consumption was negatively correlated with baseline (r = - 0.679, p = 0.001). There was no statistically significant correlation between percent change in vascular reactivity and baseline (p = 0.275). There was a positive correlation between percent change in oxygen consumption and percent change in vascular reactivity (r = 0.442, p = 0.045). In the 11 patients, RBC transfusion did not globally affect NIRS-derived variables or SDF-derived variables. There was no statistically significant correlation between percent change in small vessel perfusion and baseline perfusion (r = -0.474, p = 0.141), between percent change in small vessel flow and baseline flow (r = -0.418, p = 0.201), or between percent change in small vessel perfusion and percent change in small vessel flow (r = 0.435, p = 0.182).

Conclusions

In a small sample population, muscle tissue oxygen consumption, microvascular reactivity and sublingual microcirculation were globally unaltered by RBC transfusion in severe septic patients. However, muscle oxygen consumption improved in patients with low baseline and deteriorated in patients with preserved baseline. Future research with larger samples is needed to further examine the association between RBC transfusion and outcomes of patients resuscitated early in severe sepsis, with an emphasis on elucidating the potential contribution of microvascular factors.

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Martin GS, Mannino DM, Eaton S, Moss M: The epidemiology of sepsis in the United States from 1979 through 2000. N Engl J Med 2003, 348: 1546–1554. 10.1056/NEJMoa022139PubMedCrossRef

Brun-Buisson C, Doyon F, Carlet J: Incidence, risk factors, and outcome of severe sepsis and septic shock in adults: a multicenter prospective study in intensive care units. JAMA 1995, 274: 968–974. 10.1001/jama.274.12.968PubMedCrossRef

Karlsson S, Ruokonen E, Varpula T, Ala-Kokko TI, Pettilä V, Finnsepsis Study Group: Long-term outcome and quality-adjusted life years after severe sepsis. Crit Care Med 2009, 37: 1268–1274. 10.1097/CCM.0b013e31819c13acPubMedCrossRef

Angus DC, Linde-Zwirble WT, Lidicker J, Clermont G, Carcillo J, Pinsky MR: Epidemiology of severe sepsis in the United States: analysis of incidence, outcome, and associated costs of care. Crit Care Med 2001, 29: 1303–1310. 10.1097/00003246-200107000-00002PubMedCrossRef

Chalfin DB, Holbein ME, Fein AM, Carlon GC: Cost-effectiveness of monoclonal antibodies to gram-negative endotoxin in the treatment of gram-negative sepsis in ICU patients. JAMA 1993, 269: 249–254. 10.1001/jama.269.2.249PubMedCrossRef

Wheeler AP, Bernard GR: Treating patients with severe sepsis. N Engl J Med 1999, 340: 207–214. 10.1056/NEJM199901213400307PubMedCrossRef

Parrillo JE, Parker MM, Natanson C, Suffredini AF, Danner RL, Cunnion RE, Ognibene FP: Septic shock in humans: advances in the understanding of pathogenesis, cardiovascular dysfunction, and therapy. Ann Intern Med 1990, 113: 227–242.PubMedCrossRef

Angus DC, Wax RS: Epidemiology of sepsis: an update. Crit Care Med 2001,29(Suppl 7):S109–116.PubMedCrossRef

Comprehensive report on blood collection and transfusion in the US in 2001 [http://www.nbdrc.org] 10.1128/JCM.00635-06

10.

Vincent JL, Baron JF, 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: 1499–1507. 10.1001/jama.288.12.1499PubMedCrossRef

11.

Corwin HL, Gettinger A, Pearl RG, Fink MP, Levy MM, Abraham E, MacIntyre NR, Shabot MM, Duh MS, 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. 10.1097/01.CCM.0000104112.34142.79PubMedCrossRef

12.

Dellinger RP, Levy MM, Carlet JM, Bion J, Parker MM, Jaeschke R, Reinhart K, Angus DC, Brun-Buisson C, Beale R, Calandra T, Dhainaut JF, Gerlach H, Harvey M, Marini JJ, Marshall J, Ranieri M, Ramsay G, Sevransky J, Thompson BT, Townsend S, Vender JS, Zimmerman JL, Vincent JL: Surviving Sepsis Campaign: International guidelines for management of severe sepsis and septic shock: 2008 [published correction appears in Crit Care Med 2008; 36:1394–1396]. Crit Care Med 2008, 36: 296–327. 10.1097/01.CCM.0000298158.12101.41PubMedCrossRef

13.

Goedhart PT, Khalilzada M, Bezemer R, Merza J, Ince C: Sidestream Dark Field (SDF) imaging: a novel stroboscopic LED ring-based imaging modality for clinical assessment of the microcirculation. Optics Express 2007, 15: 15101–15114. 10.1364/OE.15.015101PubMedCrossRef

14.

De Backer D, Creteur J, Preiser JC, Dubois MJ, Vincent JL: Microvascular blood flow is altered in patients with sepsis. Am J Respir Crit Care Med 2002, 166: 98–104. 10.1164/rccm.200109-016OCPubMedCrossRef

15.

Spronk PE, Ince C, Gardien MJ, Mathura KR, Oudemans-van Straaten HM, Zandstra DF: Nitroglycerin in septic shock after intravascular volume resuscitation. Lancet 2002, 360: 1395–1396. 10.1016/S0140-6736(02)11393-6PubMedCrossRef

16.

Trzeciak S, Dellinger RP, Parrillo JE, Bajaj J, Abate NL, Arnold RC, Colilla S, Zanotti S, Hollenberg SM: Early microcirculatory perfusion derangements in patients with severe sepsis and septic shock: relationship to hemodynamics, oxygen transport, and survival. Ann Emerg Med 2007, 49: 88–98. 10.1016/j.annemergmed.2006.08.021PubMedCrossRef

17.

Sakr Y, Dubois MJ, De Backer D, Creteur J, Vincent JL: Persistant microvasculatory alterations are associated with organ failure and death in patients with septic shock. Crit Care Med 2004, 32: 1825–1831. 10.1097/01.CCM.0000138558.16257.3FPubMedCrossRef

18.

De Blasi RA, Ferrari M, Natali A, Conti G, Mega A, Gasparetto A: Noninvasive measurement of forearm blood flow and oxygen consumption by nearinfrared spectroscopy. J Appl Physiol 1994, 76: 1388–1393.PubMed

19.

De Blasi RA, Quaglia E, Ferrari M: Skeletal muscle oxygenation monitoring by near infrared spectroscopy. Biochem Int 1991, 25: 241–245.PubMed

20.

Astiz ME, DeGent GE, Lin RY, Rackow EC: Microvascular function and rheologic changes in hyperdynamic sepsis. Crit Care Med 1995, 23: 265–271. 10.1097/00003246-199502000-00011PubMedCrossRef

21.

Neviere R, Mathieu D, Chagnon JL, Lebleu N, Millien JP, Wattel F: Skeletal muscle microvascular blood flow and oxygen transport in patients with severe sepsis. Am J Respir Crit Care Med 1996, 153: 191–195.PubMedCrossRef

22.

Doerschug K, Delsing A, Schmidt G, Haynes WG: Impairments in microvascular reactivity are related to organ failure in human sepsis. Am J Physiol Heart Circ Physiol 2007, 293: H1065-H1071. 10.1152/ajpheart.01237.2006PubMedCrossRef

23.

Pareznik R, Knezevic R, Voga G, Podbregar M: Changes in muscle tissue oxygenation during stagnant ischemia in septic patients. Intensive Care Med 2006, 32: 87–92. 10.1007/s00134-005-2841-8PubMedCrossRef

24.

Creteur J, Carollo T, Soldati G, Buchele G, De Backer D, Vincent JL: The prognostic value of muscle StO2 in septic patients. Intensive Care Med 2007, 33: 1549–1556. 10.1007/s00134-007-0739-3PubMedCrossRef

25.

Skarda D, Mulier K, Myers D, Taylor JH, Beilman GJ: Dynamic Near-Infrared Spectroscopy Measurements in Patients with Severe Sepsis. Shock 2007, 27: 348–353. 10.1097/01.shk.0000239779.25775.e4PubMedCrossRef

26.

Levy MM, Fink MP, Marshall JC, Abraham E, Angus D, Cook D, Cohen J, Opal SM, Vincent JL, Ramsay G: 2001 SCCM/ESICM/ACCP/ATS/SIS International Sepsis Definitions Conference. Crit Care Med 2003, 31: 1250–1256. 10.1097/01.CCM.0000050454.01978.3BPubMedCrossRef

27.

Knaus WA, Draper EA, Wagner DP, Zimmerman JE: APACHE II: A severity of disease classification system. Crit Care Med 1985, 13: 818–829. 10.1097/00003246-198510000-00009PubMedCrossRef

28.

Vincent JL, Moreno J, Takala J, Willatts S, De Mendonça A, Bruining H, Reinhart CK, Suter PM, Thijs LG: The SOFA (Sepsis-related Organ Failure Assessment) score to describe organ dysfunction/failure. Intensive Care Med 2000, 22: 707–710.CrossRef

29.

Mulier KE, Skarda DE, Taylor JH, McGraw MK, Gallea BL, Beilman GJ: Near-infrared spectroscopy in patients with severe sepsis: correlation with invasive hemodynamic measurements. Surg Infect (Larchmt) 2008, 9: 515–519. 10.1089/sur.2007.091CrossRef

30.

Wang P, Hauptman JG, Chaudry IH: Hemorrhage produces depression in microvascular blood flow which persists despite fluid resuscitation. Circ Shock 1990, 32: 307–318.PubMed

31.

De Backer D, Hollenberg S, Boerma C, Goedhart P, Büchele G, Ospina-Tascon G, Dobbe I, Ince C: How to evaluate the microcirculation: report of a round table conference. Crit Care 2007, 11: R101. 10.1186/cc6118PubMedCentralPubMedCrossRef

32.

Dobbe JGG, Streekstra GJ, Atasever B, van Zijderveld R, Ince C: Measurement of functional microcirculatory geometry and velocity distributions using automated image analysis. Med Biol Eng Comput 2008, 46: 659–670. 10.1007/s11517-008-0349-4PubMedCentralPubMedCrossRef

33.

Hebert PC, Wells G, Blajchman MA, 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: 409–417. 10.1056/NEJM199902113400601PubMedCrossRef

34.

Vincent JL, Baron JF, Reinhart K, Gattinoni L, Thijs L, Webb A, Meier-Hellmann A, Nollet G, Peres-Bota D, ABC(Anemia and Blood Transfusion in Critical Care) Investigators: Anemia and blood transfusion in critically ill patients. JAMA 2002, 288: 1499–1507. 10.1001/jama.288.12.1499PubMedCrossRef

35.

Rivers E, Nguyen B, Havstad S, Ressler J, Muzzin A, Knoblich B, Peterson E, Tomlanovich M, for the Early Goal-Directed Therapy Collaborative Group: Early goal-directed therapy in the treatment of severe sepsis and septic shock. N Engl J Med 2001, 345: 1368–1377. 10.1056/NEJMoa010307PubMedCrossRef

36.

Powell RJ, Machiedo GW, Rush BFJ: Decreased red blood cell deformability and impaired oxygen utilization during human sepsis. Am Surg 1993, 59: 65–68.PubMed

37.

Baskurt OK, Gelmont D, Meiselman HJ: Red blood cell deformability in sepsis. Am J Respir Crit Care Med 1998, 157: 421–427.PubMedCrossRef

38.

Hurd TC, Dasmahapatra KS, Rush BFJ, Machiedo GW: Red blood cell deformability in human and experimental sepsis. Arch Surg 1988, 123: 217–220. 10.1001/archsurg.1988.01400260101012PubMedCrossRef

39.

Reggiori G, Occhipinti G, De Gasperi A, Vincent JL, Piagnerelli M: Early alterations of red blood cell rheology in critically ill patients. Crit Care Med 2009, 37: 3041–3046. 10.1097/CCM.0b013e3181b02b3fPubMedCrossRef

40.

Cosby K, Partovi KS, Crawford JH, Patel RP, Reiter CD, Martyr S, Yang BK, Waclawiw MA, Zalos G, Xu X, Huang KT, Shields H, Kim-Shapiro DB, Schechter AN, Cannon RO, Gladwin MT: Nitrite reduction to nitric oxide by deoxyhemoglobin vasodilates the human circulation. Nat Med 2003, 9: 1498–1505. 10.1038/nm954PubMedCrossRef

41.

Jia L, Bonaventura C, Bonaventura J, Stamler JS: S-nitrosohaemoglobin: a dynamic activity of blood involved in vascular control. Nature 1996, 380: 221–226. 10.1038/380221a0PubMedCrossRef

42.

Ellsworth ML: The red blood cell as an oxygen sensor: what is the evidence? Acta Physiol Scand 2000, 168: 551–559. 10.1046/j.1365-201x.2000.00708.xPubMedCrossRef

43.

Fitzgerald RD, Martin CM, Dietz GE, Doig GS, Potter RF, Sibbald WJ: Transfusing red blood cells stored in citrate phosphate dextrose adenine-1 for 28 days fails to improve tissue oxygenation in rats. Crit Care Med 1997, 25: 726–732. 10.1097/00003246-199705000-00004PubMedCrossRef

44.

Marik PE, Sibbald WJ: Effect of stored-blood transfusion on oxygen delivery in patients with sepsis. JAMA 1993, 269: 3024–3030. 10.1001/jama.269.23.3024PubMedCrossRef

45.

Raat NJ, Verhoeven AJ, Mik EG, Gouwerok CW, Verhaar R, Goedhart PT, de Korte D, Ince C: The effect of storage time of human red cells on intestinal microcirculatory oxygenation in a rat isovolemic exchange model. Crit Care Med 2005, 33: 39–45. 10.1097/01.CCM.0000150655.75519.02PubMedCrossRef

46.

Zallen G, Offner PJ, Moore EE, Blackwell J, Ciesla DJ, Gabriel J, Denny C, Silliman CC: Age of transfused blood is an independent risk factor for post injury multiple organ failure. Am J Surg 1999, 178: 570–572. 10.1016/S0002-9610(99)00239-1PubMedCrossRef

47.

Ho J, Sibbald WJ, Chin-Yee IH: Effects of storage on efficacy of red cell transfusion: When is it not safe? Crit Care Med 2003, 31: S687-S697. 10.1097/01.CCM.0000099349.17094.A3PubMedCrossRef

48.

Peek CC, Moore GL, Bolin RB: Adenine in blood preservation. Crit Rev Clin Lab Sci 2006, 18: 173–212.

49.

Tinmouth A, Fergusson D, Yee IC, ABLE Investigators, Canadian Critical Care Trials Group: Clinical consequences of red cell storage in the critically ill. Transfusion 2006, 46: 2014–2027. 10.1111/j.1537-2995.2006.01026.xPubMedCrossRef

50.

Lelubre C, Piagnerelli M, Vincent JL: Association between duration of storage of red blood cells and morbidity and mortality in adult patients: myth or reality? Transfusion 2009, 49: 1384–1394. 10.1111/j.1537-2995.2009.02211.xPubMedCrossRef

51.

Creteur J, Neves AP, Vincent JL: Near-infrared spectroscopy technique to evaluate the effects of red blood cell transfusion on tissue oxygenation. Critical Care 2009,13(Suppl 5):S11. 10.1186/cc8009PubMedCentralPubMedCrossRef

52.

Sakr Y, Chierego M, Piagnerelli M, Verdant C, Dubois MJ, Koch M, Creteur J, Gullo A, Vincent JL, De Backer D: Microvascular response to red blood cell transfusion in patients with severe sepsis. Crit Care Med 2007, 35: 1639–1644. 10.1097/01.CCM.0000269936.73788.32PubMedCrossRef

53.

De Backer D, Ospina-Tascon G, Salgado D, Favory R, Creteur J, Vincent JL: Monitoring the microcirculation in the critically ill patient: current methods and future approaches. Intensive Care Med 2010, 36: 1813–1825. 10.1007/s00134-010-2005-3PubMedCrossRef

54.

Yuruk K, Almac E, Bezemer R, Goedhart P, de Mol B, Ince C: Blood Transfusions recruit the microcirculation during cardiac surgery. Transfusion 2011, 51: 961–967. 10.1111/j.1537-2995.2010.02971.xPubMedCrossRef

55.

Friedlander MH, Simon R, Machiedo GW: The relationship of packed cell transfusion to red blood cell deformability in systemic inflammatory response syndrome patients. Shock 1998, 9: 84–88. 10.1097/00024382-199802000-00002PubMedCrossRef

56.

Klitzman B, Duling BR: Microvascular hematocrit and red cell flow in resting and contracting striated muscle. Am J Physiol 1979, 237: H481-H490.PubMed

57.

Sarelius IH, Duling BR: Direct measurement of microvessel hematocrit, red cell flux, velocity, and transit time. Am J Physiol 1982, 243: H1018-H1026.PubMed

Title: The effect of red blood cell transfusion on tissue oxygenation and microcirculation in severe septic patients
Authors: Farid Sadaka
Ravi Aggu-Sher
Katie Krause
Jacklyn O'Brien
Eric S Armbrecht
Robert W Taylor
Publication date: 01-12-2011
Publisher: Springer Paris
Published in: Annals of Intensive Care / Issue 1/2011
Electronic ISSN: 2110-5820
DOI: https://doi.org/10.1186/2110-5820-1-46

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

The effect of red blood cell transfusion on tissue oxygenation and microcirculation in severe septic patients

Abstract

Background

Methods

Results

Conclusions

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Abstract

Background

Methods

Results

Conclusions

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