Pulmonary hypertension in lambs transfused with stored blood is prevented by breathing nitric oxide

Anesthesiology

Volumn 116, Issue 3, 2012, Pages 637-647

  Baron, David M ^a   Yu, Binglan ^a   Lei, Chong ^a   Bagchi, Aranya ^a   Beloiartsev, Arkadi ^a   Stowell, Christopher P ^a   Steinbicker, Andrea U ^a   Malhotra, Rajeev ^a   Bloch, Kenneth D ^a   Zapol, Warren M ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

N(G) NITROARGININE METHYL ESTER; NITRIC OXIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD AUTOTRANSFUSION; BLOOD STORAGE; CONTROLLED STUDY; DRUG EFFECT; ENDOTHELIAL DYSFUNCTION; ERYTHROCYTE TRANSFUSION; HEMODYNAMICS; LAMB; LUNG ARTERY PRESSURE; LUNG VASOCONSTRICTION; NONHUMAN; PRIORITY JOURNAL; PULMONARY HYPERTENSION; SHEEP ERYTHROCYTE;

ADMINISTRATION, INHALATION; ANIMALS; ANIMALS, NEWBORN; ERYTHROCYTE TRANSFUSION; HYPERTENSION, PULMONARY; NITRIC OXIDE; SHEEP, DOMESTIC; TIME FACTORS;

EID: 84859100126     PISSN: 00033022     EISSN: 15281175     Source Type: Journal    
DOI: 10.1097/ALN.0b013e318246ef77     Document Type: Article

References (47)

1. Triulzi DJ, Yazer MH: Clinical studies of the effect of blood storage on patient outcomes. Transfus Apher Sci 2010; 43: 95-106
2. Kim-Shapiro DB, Lee J, Gladwin MT: Storage lesion: Role of red blood cell breakdown. Transfusion 2011; 51:844-51
3. Latham JT Jr, Bove JR, Weirich FL: Chemical and hematologic changes in stored CPDA-1 blood. Transfusion 1982; 22: 158-9 (Pubitemid 12100250)
4. Gladwin MT, Kim-Shapiro DB: Storage lesion in banked blood due to hemolysis-dependent disruption of nitric oxide homeostasis. Curr Opin Hematol 2009; 16:515-23
5. Rother RP, Bell L, Hillmen P, Gladwin MT: The clinical sequelae of intravascular hemolysis and extracellular plasma hemoglobin: A novel mechanism of human disease. JAMA 2005; 293:1653-62 (Pubitemid 40471796)
6. Reiter CD, Wang X, Tanus-Santos JE, Hogg N, Cannon RO 3rd, Schechter AN, Gladwin MT: Cell-free hemoglobin limits nitric oxide bioavailability in sickle-cell disease. Nat Med 2002; 8:1383-9 (Pubitemid 36019423)
7. Lee MT, Small T, Khan MA, Rosenzweig EB, Barst RJ, Brittenham GM: Doppler-defined pulmonary hypertension and the risk of death in children with sickle cell disease followed for a mean of three years. Br J Haematol 2009; 146:437-41
8. Minniti CP, Sable C, Campbell A, Rana S, Ensing G, Dham N, Onyekwere O, Nouraie M, Kato GJ, Gladwin MT, Castro OL, Gordeuk VR: Elevated tricuspid regurgitant jet velocity in children and adolescents with sickle cell disease: Association with hemolysis and hemoglobin oxygen desaturation. Haematologica 2009; 94:340-7
9. Yeo TW, Lampah DA, Gitawati R, Tjitra E, Kenangalem E, McNeil YR, Darcy CJ, Granger DL, Weinberg JB, Lopansri BK, Price RN, Duffull SB, Celermajer DS, Anstey NM: Impaired nitric oxide bioavailability and L-arginine reversible endothelial dysfunction in adults with falciparum malaria. J Exp Med 2007; 204:2693-704 (Pubitemid 350044792)
10. Janka JJ, Koita OA, Traoré B, Traoré JM, Mzayek F, Sachdev V, Wang X, Sanogo K, Sangaré L, Mendelsohn L, Masur H, Kato GJ, Gladwin MT, Krogstad DJ: Increased pulmonary pressures and myocardial wall stress in children with severe malaria. J Infect Dis 2010; 202:791-800
11. Morris CR, Kato GJ, Poljakovic M, Wang X, Blackwelder WC, Sachdev V, Hazen SL, Vichinsky EP, Morris SM Jr, Gladwin MT: Dysregulated arginine metabolism, hemolysis-associated pulmonary hypertension, and mortality in sickle cell disease. JAMA 2005; 294:81-90 (Pubitemid 41002842)
12. Jy W, Ricci M, Shariatmadar S, Gomez-Marin O, Horstman LH, Ahn YS: Microparticles in stored red blood cells as potential mediators of transfusion complications. Transfusion 2011; 51:886-93
13. Donadee C, Raat NJ, Kanias T, Tejero J, Lee JS, Kelley EE, Zhao X, Liu C, Reynolds H, Azarov I, Frizzell S, Meyer EM, Donnenberg AD, Qu L, Triulzi D, Kim-Shapiro DB, Gladwin MT: Nitric oxide scavenging by red blood cell microparticles and cell-free hemoglobin as a mechanism for the red cell storage lesion. Circulation 2011; 124:465-76
14. Butler AR, Megson IL, Wright PG: Diffusion of nitric oxide and scavenging by blood in the vasculature. Biochim Biophys Acta 1998; 1425:168-76 (Pubitemid 28479723)
15. Minneci PC, Deans KJ, Zhi H, Yuen PS, Star RA, Banks SM, Schechter AN, Natanson C, Gladwin MT, Solomon SB: Hemolysis-associated endothelial dysfunction mediated by accelerated NO in activation by decompartmentalized oxyhemoglobin. J Clin Invest 2005; 115:3409-17 (Pubitemid 43121829)
16. Kato GJ, McGowan V, Machado RF, Little JA, Taylor J 6th, Morris CR, Nichols JS, Wang X, Poljakovic M, Morris SM Jr, Gladwin MT: Lactate dehydrogenase as abiomarker of hemolysis-associated nitric oxide resistance, priapism, leg ulceration, pulmonary hypertension, and death in patients with sickle cell disease. Blood 2006; 107:2279-85 (Pubitemid 43345545)
17. Yu B, Shahid M, Egorina EM, Sovershaev MA, Raher MJ, Lei C, Wu MX, Bloch KD, Zapol WM: Endothelial dysfunction enhances vasoconstriction due to scavenging of nitric oxide by a hemoglobin-based oxygen carrier. ANESTHESIOLOGY 2010; 112:586-94
18. Reynolds JD, Ahearn GS, Angelo M, Zhang J, Cobb F, Stamler JS: S-nitrosohemoglobin deficiency: A mechanism for loss of physiological activity in banked blood. Proc Natl Acad Sci U S A 2007; 104:17058-62 (Pubitemid 350210991)
19. Félétou M, Vanhoutte PM: Endothelial dysfunction: A multi-faceted disorder (The Wiggers Award Lecture). Am J Physiol Heart Circ Physiol 2006; 291:H985-1002
20. Yu B, Lei C, Baron DM, Steinbicker AU, Bloch KD, Zapol WM: Diabetes augments and inhaled nitric oxide prevents the adverse hemodynamic effects of transfusing syngeneic stored blood in mice. Transfusion, In Press 2011
21. Wessel DL, Adatia I, Giglia TM, Thompson JE, Kulik TJ: Use of inhaled nitric oxide and acetylcholine in the evaluation of pulmonary hypertension and endothelial function after cardiopulmonary bypass. Circulation 1993; 88:2128-38 (Pubitemid 23326092)
22. Roberts JD Jr, Fineman JR, Morin FC 3rd, Shaul PW, Rimar S, Schreiber MD, Polin RA, Zwass MS, Zayek MM, Gross I, Heymann MA, Zapol WM: Inhaled nitric oxide and persistent pulmonary hypertension of the newborn. The Inhaled Nitric Oxide Study Group. N Engl J Med 1997; 336:605-10 (Pubitemid 27093405)
23. Yu B, Volpato GP, Chang K, Bloch KD, Zapol WM: Prevention of the pulmonary vasoconstrictor effects of HBOC-201 in awake lambs by continuously breathing nitric oxide. ANESTHESIOLOGY 2009; 110:113-22
24. Marshall C, Lindgren L, Marshall BE: Effects of halothane, enflurane, and isoflurane on hypoxic pulmonary vasoconstriction in rat lungs in vitro. ANESTHESIOLOGY 1984; 60:304-8 (Pubitemid 14172407)
25. Hulet CV, Ercanbrack SK, Knight AD: Development of the Polypay breed of sheep. J Anim Sci 1984; 58:15-24
26. Mock DM, Lankford GL, Widness JA, Burmeister LF, Kahn D, Strauss RG: Measurement of red cell survival using biotin-labeled red cells: Validation against 51Cr-labeled red cells. Transfusion 1999; 39:156-62 (Pubitemid 29085136)
27. Hansard SL: Residual organ blood volume of cattle, sheep and swine. Proc Soc Exp Biol Med 1956; 91:31-4
28. Weimann J, Ullrich R, Hromi J, Fujino Y, Clark MW, Bloch KD, Zapol WM: Sildenafil is a pulmonary vasodilator in awake lambs with acute pulmonary hypertension. ANESTHESIOLOGY 2000; 92:1702-12 (Pubitemid 30412491)
29. Sowemimo-Coker SO: Red blood cell hemolysis during processing. Transfus Med Rev 2002; 16:46-60
30. Dumont LJ, AuBuchon JP: Evaluation of proposed FDA criteria for the evaluation of radiolabeled red cell recovery trials. Transfusion 2008; 48:1053-60 (Pubitemid 351793478)
31. Bunn HF: Differences in the interaction of 2,3-diphosphoglycerate with certain mammalian hemoglobins. Science 1971; 172:1049-50
32. Kallapur SG, Nitsos I, Moss TJ, Polglase GR, Pillow JJ, Cheah FC, Kramer BW, Newnham JP, Ikegami M, Jobe AH: IL-1 mediates pulmonary and systemic inflammatory responses to chorioamnionitis induced by lipopolysaccharide. Am J Respir Crit Care Med 2009; 179:955-61
33. Staub NC: Pulmonary intravascular macrophages. Annu Rev Physiol 1994; 56:47-67
34. Weitzberg E, Hezel M, Lundberg JO: Nitrate-nitrite-nitric oxide pathway: Implications for anesthesiology and intensive care. ANESTHESIOLOGY 2010; 113:1460-75
35. Gilson CR, Kraus TS, Hod EA, Hendrickson JE, Spitalnik SL, Hillyer CD, Shaz BH, Zimring JC: A novel mouse model of red blood cell storage and posttransfusion in vivo survival. Transfusion 2009; 49:1546-53
36. Hod EA, Zhang N, Sokol SA, Wojczyk BS, Francis RO, Ansaldi D, Francis KP, Della-Latta P, Whittier S, Sheth S, Hendrickson JE, Zimring JC, Brittenham GM, Spitalnik SL: Transfusion of red blood cells after prolonged storage produces harmful effects that are mediated by iron and inflammation. Blood 2010; 115:4284-92
37. Shemin D, Rittenberg D: The life span of the human red blood cell. J Biol Chem 1946; 166:627-36
38. Giles RC Jr, Berman A, Hildebrandt PK, McCaffrey RP: The use of51Cr for sheep red blood cell survival studies. Proc Soc Exp Biol Med 1975; 148:795-8
39. Gao Y, Raj JU: Regulation of the pulmonary circulation in the fetus and newborn. Physiol Rev 2010; 90:1291-335
40. Rasmusen BA: Blood groups in sheep. Ann N Y Acad Sci 1962; 97:306-19
41. Grimshaw K, Sahler J, Spinelli SL, Phipps RP, Blumberg N: New frontiers intransfusion biology: Identification and significance of mediators of morbidity and mortality in stored red blood cells. Transfusion 2011; 51:874-80
42. Blood AB, Schroeder HJ, Terry MH, Merrill-Henry J, Bragg SL, Vrancken K, Liu T, Herring JL, Sowers LC, Wilson SM, Power GG: Inhaled nitrite reverses hemolysis-induced pulmonary vasoconstriction in newborn lambs without blood participation. Circulation 2011; 123:605-12
43. Boretti FS, Buehler PW, D'Agnillo F, Kluge K, Glaus T, Butt OI, Jia Y, Goede J, Pereira CP, Maggiorini M, Schoedon G, Alayash AI, Schaer DJ: Sequestration of extracellular hemoglobin within a haptoglobin complex decreases its hypertensive and oxidative effects in dogs and guinea pigs. J Clin Invest 2009; 119:2271-80
44. Yu B, Raher MJ, Volpato GP, Bloch KD, Ichinose F, Zapol WM: Inhaled nitric oxide enables artificial blood transfusion without hypertension. Circulation 2008; 117:1982-90 (Pubitemid 351543474)
45. Frostell C, Fratacci MD, Wain JC, Jones R, Zapol WM: Inhaled nitric oxide. A selective pulmonary vasodilator reversing hypoxic pulmonary vasoconstriction. Circulation 1991; 83: 2038-47
46. Stamler JS, Jia L, Eu JP, McMahon TJ, Demchenko IT, Bonaventura J, Gernert K, Piantadosi CA: Blood flow regulation by S-nitrosohemoglobin in the physiological oxygen gradient. Science 1997; 276:2034-7 (Pubitemid 27443606)
47. Hendrickson JE, Hod EA, Cadwell CM, Eisenbarth SC, Spiegel DA, Tormey CA, Spitalnik SL, Zimring JC: Rapid clearance of transfused murine red blood cells is associated with recipient cytokine storm and enhanced alloimmunogenicity. Transfusion 2011; 51:2445-54