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Annual Review of Biomedical Engineering

Volume 16, 2014

Blood Substitutes

Abstract

The toxic side effects of early generations of red blood cell substitutes have stimulated development of more safe and efficacious high-molecular-weight polymerized hemoglobins, poly(ethylene glycol)-conjugated hemoglobins, and vesicle-encapsulated hemoglobins. Unfortunately, the high colloid osmotic pressure and blood plasma viscosity of these new-generation materials limit their application to blood concentrations that, in general, are not sufficient for full restoration of oxygen-carrying and -delivery capacity. However, these materials may serve as oxygen therapeutics for treating tissues affected by ischemia and trauma, particularly when the therapeutics are coformulated with antioxidants. These new oxygen therapeutics also possess additional beneficial effects owing to their optimal plasma expansion properties, which induce systemic supraperfusion that increases endothelial nitric oxide production and improves tissue washout of metabolic wastes, further contributing to their therapeutic role.

Keyword(s): oxygen therapeutics, plasma expanders, poly(ethylene glycol)-conjugated hemoglobin, polymerized hemoglobin, red blood cell substitutes, supraperfusion, vesicle-encapsulated hemoglobin
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2014-07-11
2024-04-26
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Literature Cited

  1. Greening DW, Glenister KM, Sparrow RL, Simpson RJ. 1.  2010. International blood collection and storage: clinical use of blood products. J. Proteomics 73:386–95 [Google Scholar]
  2. Wang J, Guo N, Guo X, Li J, Wen G-X. 2.  et al. 2010. Who donates blood at five ethnically and geographically diverse blood centers in China in 2008. Transfusion 50:2686–94 [Google Scholar]
  3. Seifried E, Mueller MM. 3.  2011. The present and future of transfusion medicine. Blood Transfus. 9:371–76 [Google Scholar]
  4. Morley S. 4.  2009. Red blood cell transfusions in acute paediatrics. Arch. Dis. Child. Educ. Pract. Ed. 94:65–73 [Google Scholar]
  5. Cobain TJ, Vamvakas EC, Wells A, Titlestad K. 5.  2007. A survey of the demographics of blood use. Transfus. Med. 17:1–15 [Google Scholar]
  6. Shander A, Hofmann A, Ozawa S, Theusinger OM, Gombotz H, Spahn DR. 6.  2010. Activity-based costs of blood transfusions in surgical patients at four hospitals. Transfusion 50:753–65 [Google Scholar]
  7. Seifried E, Klueter H, Weidmann C, Staudenmaier T, Schrezenmeier H. 7.  et al. 2011. How much blood is needed?. Vox Sang. 100:10–21 [Google Scholar]
  8. Koch CG, Li L, Sessler DI, Figueroa P, Hoeltge GA. 8.  et al. 2008. Duration of red-cell storage and complications after cardiac surgery. N. Engl. J. Med. 358:1229–39 [Google Scholar]
  9. Shiba H, Ishida Y, Wakiyama S, Iida T, Matsumoto M. 9.  et al. 2009. Negative impact of blood transfusion on recurrence and prognosis of hepatocellular carcinoma after hepatic resection. J. Gastrointest. Surg. 13:1636–42 [Google Scholar]
  10. van de Watering L, Lorinser J, Versteegh M, Westendord R, Brand A. 10.  2006. Effects of storage time of red blood cell transfusions on the prognosis of coronary artery bypass graft patients. Transfusion 46:1712–18 [Google Scholar]
  11. Sparrow RL. 11.  2010. Red blood cell storage and transfusion-related immunomodulation. Blood Transfus. 8:Suppl. 3s26–30 [Google Scholar]
  12. Baskurt OK, Meiselman HJ. 12.  2003. Blood rheology and hemodynamics. Semin. Thromb. Hemost. 29:435–50 [Google Scholar]
  13. Tsai AG, Hofmann A, Cabrales P, Intaglietta M. 13.  2010. Perfusion versus oxygen delivery in transfusion with “fresh” and “old” red blood cells: the experimental evidence. Transfus. Apher. Sci. 43:69–78 [Google Scholar]
  14. Berezina TL, Zaets SB, Morgan C, Spillert CR, Kamiyama M. 14.  et al. 2002. Influence of storage on red blood cell rheological properties. J. Surg. Res. 102:6–12 [Google Scholar]
  15. Vicente JR, Croci AT, Camargo OP. 15.  2008. Blood loss in the minimally invasive posterior approach to total hip arthroplasty: a comparative study. Clinics (Sao Paulo) 63:351–56 [Google Scholar]
  16. Smith TO, Blake V, Hing CB. 16.  2011. Minimally invasive versus conventional exposure for total hip arthroplasty: a systematic review and meta-analysis of clinical and radiological outcomes. Int. Orthop. 35:173–84 [Google Scholar]
  17. Troisi RI, Patriti A, Montalti R, Casciola L. 17.  2013. Robot assistance in liver surgery: a real advantage over a fully laparoscopic approach? Results of a comparative bi-institutional analysis. Int. J. Med. Robot. 9:160–66 [Google Scholar]
  18. Frank SM, Savage WJ, Rothschild JA, Rivers RJ, Ness PM. 18.  et al. 2012. Variability in blood and blood component utilization as assessed by an anesthesia information management system. Anesthesiology 117:99–106 [Google Scholar]
  19. Napolitano LM, Kurek S, Luchette FA, Anderson GL, Bard MR. 19.  et al. 2009. Clinical practice guideline: red blood cell transfusion in adult trauma and critical care. J. Trauma 67:1439–42 [Google Scholar]
  20. Wier LM, Pfuntner A, Maeda J, Stranges E, Ryan K. 20.  2011. HCUP Facts and Figures: Statistics on Hospital-Based Care in the United States, 2009 Rockville, MD: Agency Healthc. Res. Qual.
  21. Whitaker BI. 21.  2013. The 2011 national blood collection and utilization survey report OMB 0990–0313, US Dep. Health Hum. Serv., Washington, DC
  22. Stramer SL. 22.  2007. Current risks of transfusion-transmitted agents: a review. Arch. Pathol. Lab. Med. 131:702–7 [Google Scholar]
  23. Allain JP, Stramer SL, Carneiro-Proietti AB, Martins ML, Lopes da Silva SN. 23.  et al. 2009. Transfusion-transmitted infectious diseases. Biologicals 37:71–77 [Google Scholar]
  24. Isbister JP. 24.  2012. Comparing apples with oranges. Vox Sang. 103:359–60 [Google Scholar]
  25. Isbister JP, Shander A, Spahn DR, Erhard J, Farmer SL, Hofmann A. 25.  2011. Adverse blood transfusion outcomes: establishing causation. Transf. Med. Rev. 25:89–101 [Google Scholar]
  26. Hofmann A, Ozawa S, Farrugia A, Farmer SL, Shander A. 26.  2013. Economic considerations on transfusion medicine and patient blood management. Best Pract. Res. Clin. Anaesthesiol. 27:59–68 [Google Scholar]
  27. Shander A, Fink A, Javidroozi M, Erhard J, Farmer SL. 27.  et al. 2011. Appropriateness of allogeneic red blood cell transfusion: the international consensus conference on transfusion outcomes. Transfus. Med. Rev. 25:232–46.e53 [Google Scholar]
  28. Rao SV, Jollis JG, Harrington RA, Granger CB, Newby LK. 28.  et al. 2004. Relationship of blood transfusion and clinical outcomes in patients with acute coronary syndromes. JAMA 292:1555–62 [Google Scholar]
  29. Doyle BJ, Rihal CS, Gastineau DA, Holmes DR Jr. 29.  2009. Bleeding, blood transfusion, and increased mortality after percutaneous coronary intervention: implications for contemporary practice. J. Am. Coll. Cardiol. 53:2019–27 [Google Scholar]
  30. Aronson D, Dann EJ, Bonstein L, Blich M, Kapeliovich M. 30.  et al. 2008. Impact of red blood cell transfusion on clinical outcomes in patients with acute myocardial infarction. Am. J. Cardiol. 102:115–19 [Google Scholar]
  31. Casutt M, Seifert B, Pasch T, Schmid ER, Turina MI, Spahn DR. 31.  1999. Factors influencing the individual effects of blood transfusions on oxygen delivery and oxygen consumption. Crit. Care Med. 27:2194–200 [Google Scholar]
  32. Raat NJ, Verhoeven AJ, Mik EG, Gouwerok CW, Verhaar R. 32.  et al. 2005. The effect of storage time of human red cells on intestinal microcirculatory oxygenation in a rat isovolemic exchange model. Crit. Care Med. 33:39–45;238–89 [Google Scholar]
  33. Bernard AC, Davenport DL, Chang PK, Vaughan TB, Zwischenberger JB. 33.  2009. Intraoperative transfusion of 1 U to 2 U packed red blood cells is associated with increased 30-day mortality, surgical-site infection, pneumonia, and sepsis in general surgery patients. J. Am. Coll. Surg. 208:931–39 [Google Scholar]
  34. Sugita S, Sasaki A, Iwaki K, Uchida H, Kai S. 34.  et al. 2008. Prognosis and postoperative lymphocyte count in patients with hepatocellular carcinoma who received intraoperative allogenic blood transfusion: a retrospective study. Eur. J. Surg. Oncol. 34:339–45 [Google Scholar]
  35. Zhu H, Zennadi R, Xu BX, Eu JP, Torok JA. 35.  et al. 2011. Impaired adenosine-5′-triphosphate release from red blood cells promotes their adhesion to endothelial cells: a mechanism of hypoxemia after transfusion. Crit. Care Med. 39:2478–86 [Google Scholar]
  36. Wang D, Sun J, Solomon SB, Klein HG, Natanson C. 36.  2012. Transfusion of older stored blood and risk of death: a meta-analysis. Transfusion 52:1184–95 [Google Scholar]
  37. LeLubre C, Vincent JL. 37.  2011. Red blood cell transfusion in the critically ill patient. Ann. Intensive Care 1:43 [Google Scholar]
  38. Saugel B, Klein M, Hapfelmeier A, Phillip V, Schultheiss C. 38.  et al. 2013. Effects of red blood cell transfusion on hemodynamic parameters: a prospective study in intensive care unit patients. Scand. J. Trauma Resusc. Emerg. Med. 21:21 [Google Scholar]
  39. Martini J, Carpentier B, Chávez Negrete A, Frangos JA, Intaglietta M. 39.  2005. Paradoxical hypotension following increased hematocrit and blood viscosity. Am. J. Physiol. Heart Circ. Physiol. 289:5H2136–43 [Google Scholar]
  40. Salazar Vázquez BY, Cabrales P, Tsai AG, Johnson PC, Intaglietta M. 40.  2008. Lowering of blood pressure by increasing hematocrit with non–nitric oxide–scavenging red blood cells. Am. J. Respir. Cell Mol. Biol. 38:135–42 [Google Scholar]
  41. Vázquez BY, Martini J, Chávez-Negrete A, Cabrales P, Tsai AG, Intaglietta M. 41.  Salazar 2009. Microvascular benefits of increasing plasma viscosity and maintaining blood viscosity: counterintuitive experimental findings. Biorheology 46:167–79 [Google Scholar]
  42. Cotton BA, Guy JS, Morris JA Jr, Abumrad NN. 42.  2006. The cellular, metabolic, and systemic consequences of aggressive fluid resuscitation strategies. Shock 26:115–21 [Google Scholar]
  43. Cabrales P, Intaglietta M, Tsai AG. 43.  2005. Increase plasma viscosity sustains microcirculation after resuscitation from hemorrhagic shock and continuous bleeding. Shock 23:549–55 [Google Scholar]
  44. Kerger H, Saltzman DJ, Menger MD, Messmer K, Intaglietta M. 44.  1996. Systemic and subcutaneous microvascular Po2 dissociation during 4-h hemorrhagic shock in conscious hamsters. Am. J. Physiol. Heart Circ. Physiol. 270:H827–36 [Google Scholar]
  45. Silverman TA, Weiskopf RB. 45.  2009. Hemoglobin-based oxygen carriers: current status and future directions. Transfusion 49:2495–515 [Google Scholar]
  46. Mazzoni MC, Borgström P, Intaglietta M, Arfors KE. 46.  1989. Lumenal narrowing and endothelial cell swelling in skeletal muscle capillaries during hemorrhagic shock. Circ. Shock 29:27–39 [Google Scholar]
  47. Valko M, Leibfritz D, Moncol J, Cronin MT, Mazur M, Telser J. 47.  2007. Free radicals and antioxidants in normal physiological functions and human disease. Int. J. Biochem. Cell Biol. 39:44–84 [Google Scholar]
  48. Yang W, Hekimi S. 48.  2010. A mitochondrial superoxide signal triggers increased longevity in Caenorhabditis elegans. PLoS Biol. 8:e1000556 [Google Scholar]
  49. Chen JY, Scerbo M, Kramer G. 49.  2009. A review of blood substitutes: examining the history, clinical trial results, and ethics of hemoglobin-based oxygen carriers. Clinics (Sao Paulo) 64:803–13 [Google Scholar]
  50. Napolitano LM. 50.  2011. Acute traumatic hemorrhage and anemia. Chemistry and Biochemistry of Oxygen Therapeutics: From Transfusion to Artificial Blood A Mozzarelli, S Bettati 79–106 Chichester, UK: Wiley [Google Scholar]
  51. Grethlein SJ, Rajan A, Sandler SG, Talavera F, Conrad ME. 51.  et al. 2012. Blood substitutes Medscape, WebMD, New York. http://emedicine.medscape.com/article/207801
  52. Cabrales P, Intaglietta M. 52.  2013. Blood substitutes: evolution from noncarrying to oxygen- and gas-carrying fluids. ASAIO J. 59:337–54 [Google Scholar]
  53. Winslow RM. 53.  2006. Blood Substitutes London/Burlington, MA: Elsevier/Academic576
  54. Sazama K. 54.  2007. The ethics of blood management. Vox Sang. 92:95–102 [Google Scholar]
  55. Cabrales P, Intaglietta M, Tsai AG. 55.  2007. Transfusion restores blood viscosity and reinstates microvascular conditions from hemorrhagic shock independent of oxygen carrying capacity. Resuscitation 75:124–34 [Google Scholar]
  56. Chatpun S, Cabrales P. 56.  2010. Effects of plasma viscosity modulation on cardiac function during moderate hemodilution. Asian J. Transfus. Sci. 4:102–8 [Google Scholar]
  57. Tsai AG, Acero C, Nance PR, Cabrales P, Frangos JA. 57.  et al. 2005. Elevated plasma viscosity in extreme hemodilution increases perivascular nitric oxide concentration and microvascular perfusion. Am. J. Physiol. Heart Circ. Physiol. 288:H1730–39 [Google Scholar]
  58. Cabrales P, Tsai AG, Intaglietta M. 58.  2007. Hemorrhagic shock resuscitation with carbon monoxide saturated blood. Resuscitation 72:306–18 [Google Scholar]
  59. Salazar Vázquez BY, Wettstein R, Cabrales P, Tsai AG, Intaglietta M. 59.  2008. Microvascular experimental evidence on the relative significance of restoring oxygen carrying capacity versus blood viscosity in shock resuscitation. Biochim. Biophys. Acta 1784:1421–27 [Google Scholar]
  60. Messmer C, Yalcin O, Palmer AF, Cabrales P. 60.  2012. Small-volume resuscitation from hemorrhagic shock with polymerized human serum albumin. Am. J. Emerg. Med. 30:1336–46 [Google Scholar]
  61. Santry HP, Alam HB. 61.  2010. Fluid resuscitation: past, present, and the future. Shock 33:229–41 [Google Scholar]
  62. Martini J, Cabrales P, Tsai AG, Intaglietta M. 62.  2006. Mechanotransduction and the homeostatic significance of maintaining blood viscosity in hypotension, hypertension and haemorrhage. J. Intern. Med. 259:364–72 [Google Scholar]
  63. Cabrales P, Tsai AG, Intaglietta M. 63.  2004. Microvascular pressure and functional capillary density in extreme hemodilution with low- and high-viscosity dextran and a low-viscosity Hb-based O2 carrier. Am. J. Physiol. Heart Circ. Physiol. 287:H363–73 [Google Scholar]
  64. Salazar Vázquez BY. 64.  2012. Blood pressure and blood viscosity are not correlated in normal healthy subjects. Vasc. Health Risk Manag. 8:1–6 [Google Scholar]
  65. Sriram K, Tsai AG, Cabrales P, Meng F, Acharya SA. 65.  et al. 2012. PEG-albumin supraplasma expansion is due to increased vessel wall shear stress induced by blood viscosity shear thinning. Am. J. Physiol. Heart Circ. Physiol. 302:12H2489–97 [Google Scholar]
  66. Yalcin O, Wang Q, Johnson PC, Palmer AF, Cabrales P. 66.  2011. Plasma expander viscosity effects on red cell-free layer thickness after moderate hemodilution. Biorheology 48:277–91 [Google Scholar]
  67. Hightower CM, Salazar Vázquez BY, Cabrales P, Tsai AG, Acharya SA, Intaglietta M. 67.  2013. Plasma expander and blood storage effects on capillary perfusion in transfusion after hemorrhage. Transfusion 53:49–59 [Google Scholar]
  68. Mirhashemi S, Ertefai S, Messmer K, Intaglietta M. 68.  1987. Model analysis of the enhancement of tissue oxygenation by hemodilution due to increased microvascular flow velocity. Microvasc. Res. 34:290–301 [Google Scholar]
  69. Rohlfs RJ, Brunner E, Chiu A, Gonzales A, Gonzales ML. 69.  et al. 1998. Arterial blood pressure responses to cell-free hemoglobin solutions and the reaction with nitric oxide. J. Biol. Chem. 273:12128–34 [Google Scholar]
  70. Cabrales P, Tsai AG, Intaglietta M. 70.  2008. Balance between vasoconstriction and enhanced oxygen delivery. Transfusion 48:2087–95 [Google Scholar]
  71. Vandegriff KD, Winslow RM. 71.  2009. Hemospan: design principles for a new class of oxygen therapeutic. Artif. Organs 33:133–38 [Google Scholar]
  72. Hangai-Hoger N, Tsai AG, Cabrales P, Suematsu M, Intaglietta M. 72.  2007. Microvascular and systemic effects following top load administration of saturated carbon monoxide-saline solution. Crit. Care Med. 35:1123–32 [Google Scholar]
  73. Wilcox CS, Pearlman A. 73.  2008. Chemistry and antihypertensive effects of tempol and other nitroxides. Pharmacol. Rev. 60:418–69 [Google Scholar]
  74. Buehler PW, Baek JH, Lisk C, Connor I, Sullivan T. 74.  et al. 2012. Free hemoglobin induction of pulmonary vascular disease: evidence for an inflammatory mechanism. Am. J. Physiol. Lung Cell. Mol. Physiol. 303:L312–26 [Google Scholar]
  75. Kentner R, Safar P, Behringer W, Wu X, Henchir J. 75.  et al. 2007. Small volume resuscitation with tempol is detrimental during uncontrolled hemorrhagic shock in rats. Resuscitation 72:295–305 [Google Scholar]
  76. Hsia CJC, Ma L. 76.  2012. A hemoglobin-based multifunctional therapeutic: polynitroxylated pegylated hemoglobin. Artif. Organs 36:215–20 [Google Scholar]
  77. Sakai H, Tomiyama KI, Sou K, Takeoka S, Tsuchida E. 77.  2000. Poly(ethylene glycol)-conjugation and deoxygenation enable long-term preservation of hemoglobin-vesicles as oxygen carriers in a liquid state. Bioconjug. Chem. 11:425–32 [Google Scholar]
  78. Phillips WT, Klipper RW, Awasthi VD, Rudolph AS, Cliff R. 78.  et al. 1999. Polyethylene glycol-modified liposome-encapsulated hemoglobin: a long circulating red cell substitute. J. Pharmacol. Exp. Ther. 288:665–70 [Google Scholar]
  79. Shimada K, Matsuo S, Sadzuka Y, Miyagishima A, Nozawa Y. 79.  et al. 2000. Determination of incorporated amounts of poly(ethylene glycol)-derivatized lipids in liposomes for the physicochemical characterization of stealth liposomes. Int. J. Pharm. 203:255–63 [Google Scholar]
  80. Photos PJ, Bacakova L, Discher B, Bates FS, Discher DE. 80.  2003. Polymer vesicles in vivo: correlations with PEG molecular weight. J. Control Release 90:323–34 [Google Scholar]
  81. Szebeni J, Spielberg H, Cliff RO, Wassef NM, Rudolph AS, Alving CR. 81.  1997. Complement activation and thromboxane secretion by liposome-encapsulated hemoglobin in rats in vivo: inhibition by soluble complement receptor type 1. Artif. Cells Blood Substit. Immobil. Biotechnol. 25:347–55 [Google Scholar]
  82. Moghimi SM, Szebeni J. 82.  2003. Stealth liposomes and long circulating nanoparticles: critical issues in pharmacokinetics, opsonization and protein-binding properties. Prog. Lipid Res. 42:463–78 [Google Scholar]
  83. Mosqueira VC, Legrand P, Gulik A, Bourdon O, Gref R. 83.  et al. 2001. Relationship between complement activation, cellular uptake and surface physicochemical aspects of novel PEG-modified nanocapsules. Biomaterials 22:2967–79 [Google Scholar]
  84. Arifin DR, Palmer AF. 84.  2005. Polymersome encapsulated hemoglobin: a novel type of oxygen carrier. Biomacromolecules 6:2172–81 [Google Scholar]
  85. Rameez S, Alosta H, Palmer AF. 85.  2008. Biocompatible and biodegradable polymersome encapsulated hemoglobin: a potential oxygen carrier. Bioconjug. Chem. 19:1025–32 [Google Scholar]
  86. Rameez S, Banerjee U, Fontes J, Roth A, Palmer AF. 86.  2012. The reactivity of polymersome encapsulated hemoglobin with physiologically important gaseous ligands: oxygen, carbon monoxide and nitric oxide. Macromolecules 45:2385–89 [Google Scholar]
  87. Lee JC, Bermudez H, Discher BM, Sheehan MA, Won YY. 87.  et al. 2001. Preparation, stability, and in vitro performance of vesicles made with diblock copolymers. Biotechnol. Bioeng. 73:135–45 [Google Scholar]
  88. Ahmed F, Pakunlu RI, Srinivas G, Brannan A, Bates F. 88.  et al. 2006. Shrinkage of a rapidly growing tumor by drug-loaded polymersomes: pH-triggered release through copolymer degradation. Mol. Pharm. 3:340–50 [Google Scholar]
  89. Elmer J, Zorc K, Rameez S, Zhou Y, Cabrales P, Palmer AF. 89.  2012. Hypervolemic infusion of Lumbricus terrestris erythrocruorin purified by tangential-flow filtration. Transfusion 52:1729–40 [Google Scholar]
  90. Sakai H, Hara H, Yuasa M, Tsai AG, Takeoka S. 90.  et al. 2000. Molecular dimensions of Hb-based O2 carriers determine constriction of resistance arteries and hypertension. Am. J. Physiol. Heart Circ. Physiol. 279:H908–15 [Google Scholar]
  91. Cabrales P, Sun G, Zhou Y, Harris DR, Tsai AG. 91.  et al. 2009. Effects of the molecular mass of tense-state polymerized bovine hemoglobin on blood pressure and vasoconstriction. J. Appl. Physiol. 107:1548–58 [Google Scholar]
  92. Cabrales P, Sakai H, Tsai AG, Takeoka S, Tsuchida E, Intaglietta M. 92.  2005. Oxygen transport by low and normal oxygen affinity hemoglobin vesicles in extreme hemodilution. Am. J. Physiol. Heart Circ. Physiol. 288:H1885–92 [Google Scholar]
  93. Taguchi K, Urata Y, Anraku M, Watanabe H, Kadowaki D. 93.  et al. 2009. Hemoglobin vesicles, polyethylene glycol (PEG)ylated liposomes developed as a red blood cell substitute, do not induce the accelerated blood clearance phenomenon in mice. Drug Metab. Dispos. 37:2197–203 [Google Scholar]
  94. Sakai H, Sato A, Takeoka S, Tsuchida E. 94.  2009. Mechanism of flocculate formation of highly concentrated phospholipid vesicles suspended in a series of water-soluble biopolymers. Biomacromolecules 10:2344–50 [Google Scholar]
  95. Sakai H, Hara H, Yuasa M, Tsai AG, Takeoka S. 95.  et al. 2000. Molecular dimensions of Hb-based O2 carriers determine constriction of resistance arteries and hypertension. Am. J. Physiol. Heart Circ. Physiol. 279:H908–15 [Google Scholar]
  96. Sakai H, Masada Y, Onuma H, Takeoka S, Tsuchida E. 96.  2004. Reduction of methemoglobin via electron transfer from photoreduced flavin: restoration of O2-binding of concentrated hemoglobin solution coencapsulated in phospholipid vesicles. Bioconjug. Chem. 15:1037–45 [Google Scholar]
  97. Sakai H, Sato A, Takeoka S, Tsuchida E. 97.  2007. Rheological properties of hemoglobin vesicles (artificial oxygen carriers) suspended in a series of plasma-substitute solutions. Langmuir 23:8121–28 [Google Scholar]
  98. Sakai H, Sou K, Horinouchi H, Kobayashi K, Tsuchida E. 98.  2010. Hemoglobin-vesicle, a cellular artificial oxygen carrier that fulfils the physiological roles of the red blood cell structure. Adv. Exp. Med. Biol. 662:433–38 [Google Scholar]
  99. Sakai H, Sou K, Tsuchida E. 99.  2009. Hemoglobin-vesicles as an artificial oxygen carrier. Methods Enzymol. 465:363–84 [Google Scholar]
  100. Chang TM. 100.  2000. Artificial cell biotechnology for medical applications. Blood Purif. 18:91–96 [Google Scholar]
  101. Yubisui T, Matsuki T, Tanishima K, Takeshita M, Yoneyama Y. 101.  1977. NADPH-flavin reductase in human erythrocytes and the reduction of methemoglobin through flavin by the enzyme. Biochem. Biophys. Res. Commun. 76:174–82 [Google Scholar]
  102. Kuma F. 102.  1981. Properties of methemoglobin reductase and kinetic study of methemoglobin reduction. J. Biol. Chem. 256:5518–23 [Google Scholar]
  103. Scott MD, Lubin BH, Zuo L, Kuypers FA. 103.  1991. Erythrocyte defense against hydrogen peroxide: preeminent importance of catalase. J. Lab. Clin. Med. 118:7–16 [Google Scholar]
  104. Liu X, Miller MJ, Joshi MS, Sadowska-Krowicka H, Clark DA, Lancaster JR Jr. 104.  1998. Diffusion-limited reaction of free nitric oxide with erythrocytes. J. Biol. Chem. 273:18709–13 [Google Scholar]
  105. Bunn HF, Briehl RW. 105.  1970. The interaction of 2,3-diphosphoglycerate with various human hemoglobins. J. Clin. Invest. 49:1088–95 [Google Scholar]
  106. Chiancone E. 106.  1968. Dissociation of hemoglobin into subunits. II. Human oxyhemoglobin: gel filtration studies. J. Biol. Chem. 243:1212–19 [Google Scholar]
  107. Royer WE Jr, Sharma H, Strand K, Knapp JE, Bhyravbhatla B. 107.  2006. Lumbricus erythrocruorin at 3.5 Å resolution: architecture of a megadalton respiratory complex. Structure 14:1167–77 [Google Scholar]
  108. Fushitani K, Matsuura MS, Riggs AF. 108.  1988. The amino acid sequences of chains a, b, and c that form the trimer subunit of the extracellular hemoglobin from Lumbricus terrestris. J. Biol. Chem. 263:6502–17 [Google Scholar]
  109. Strand K, Knapp JE, Bhyravbhatla B, Royer WE Jr. 109.  2004. Crystal structure of the hemoglobin dodecamer from Lumbricus erythrocruorin: allosteric core of giant annelid respiratory complexes. J. Mol. Biol. 344:119–34 [Google Scholar]
  110. Sharma PK, Kuchumov AR, Chottard G, Martin PD, Wall JS, Vinogradov SN. 110.  1996. The role of the dodecamer subunit in the dissociation and reassembly of the hexagonal bilayer structure of Lumbricus terrestris hemoglobin. J. Biol. Chem. 271:8754–62 [Google Scholar]
  111. Stellwagen E. 111.  1978. Haem exposure as the determinate of oxidation-reduction potential of haem proteins. Nature 275:73–4 [Google Scholar]
  112. Harrington JP, Kobayashi S, Dorman SC, Zito SL, Hirsch RE. 112.  2007. Acellular invertebrate hemoglobins as model therapeutic oxygen carriers: unique redox potentials. Artif. Cells Blood Substit. Immobil. Biotechnol. 35:53–67 [Google Scholar]
  113. Dorman SC, Harrington JP, Martin MS, Johnson TV. 113.  2004. Determination of the formal reduction potential of Lumbricus terrestris hemoglobin using thin layer spectroelectrochemistry. J. Inorg. Biochem. 98:185–88 [Google Scholar]
  114. Dorman SC, Kenny CF, Miller L, Hirsch RE, Harrington JP. 114.  2002. Role of redox potential of hemoglobin-based oxygen carriers on methemoglobin reduction by plasma components. Artif. Cells Blood Substit. Immobil. Biotechnol. 30:39–51 [Google Scholar]
  115. Rousselot M, Delpy E, La Rochelle CD, Lagente V, Pirow R. 115.  et al. 2006. Arenicola marina extracellular hemoglobin: a new promising blood substitute. Biotechnol. J. 1:333–45 [Google Scholar]
  116. Liochev SI, Kuchumov AR, Vinogradov SN, Fridovich I. 116.  1996. Superoxide dismutase activity in the giant hemoglobin of the earthworm, Lumbricus terrestris. Arch. Biochem. Biophys. 330:281–84 [Google Scholar]
  117. Zal F, Green BN, Lallier FH, Vinogradov SN, Toulmond A. 117.  1997. Quaternary structure of the extracellular haemoglobin of the lugworm Arenicola marina: a multi-angle-laser-light-scattering and electrospray-ionisation-mass-spectrometry analysis. Eur. J. Biochem./FEBS 243:1–285–92 [Google Scholar]
  118. Thuillier R, Dutheil D, Trieu MT, Mallet V, Allain G. 118.  et al. 2011. Supplementation with a new therapeutic oxygen carrier reduces chronic fibrosis and organ dysfunction in kidney static preservation. Am. J. Transplant. 11:1845–60 [Google Scholar]
  119. Tsai AG, Intaglietta M, Sakai H, Delpy E, La Rochelle CD. 119.  et al. 2012. Microcirculation and NO-CO studies of a natural extracellular hemoglobin developed for an oxygen therapeutic carrier. Curr. Drug Discov. Technol. 9:166–72 [Google Scholar]
  120. Riess JG. 120.  2001. Oxygen carriers (“blood substitutes”)—raison d'etre, chemistry, and some physiology. Chem. Rev. 101:2797–920 [Google Scholar]
  121. Kjellström BT. 121.  2003. Blood substitutes: Where do we stand today?. J. Intern. Med. 253:495–97 [Google Scholar]
  122. Hill SE. 122.  2001. Oxygen therapeutics: current concepts. Can. J. Anesth. 48:S32–40 [Google Scholar]
  123. Klein HG. 123.  2002. Blood substitutes: how close to a solution?. Oncology 16:147–51 [Google Scholar]
  124. Stowell CP. 124.  2002. Hemoglobin-based oxygen carriers. Curr. Opin. Hematol. 9:537–43 [Google Scholar]
  125. Winslow RM. 125.  2003. Current status of blood substitute research: towards a new paradigm. J. Intern. Med. 253:508–17 [Google Scholar]
  126. Keipert PE. 126.  2003. Oxygen therapeutics (“blood substitutes”): Where are they, and what can we expect?. Adv. Exp. Med. Biol. 540:207–13 [Google Scholar]
  127. Verdin-Vasquez RC, Zepeda-Perez C, Ferra-Ferrer R, Chavez-Negrete A, Contreras F, Barroso-Aranda J. 127.  2006. Use of perftoran emulsion to decrease allogeneic blood transfusion in cardiac surgery: clinical trial. Artif. Cells Blood Substit. Immobil. Biotechnol. 34:433–54 [Google Scholar]
  128. Riess JG. 128.  2006. Perfluorocarbon-based oxygen delivery. Artif. Cells Blood Substit. Immobil. Biotechnol. 34:567–80 [Google Scholar]
  129. Doherty DH, Doyle MP, Curry SR, Vali RJ, Fattor TJ. 129.  et al. 1998. Rate of reaction with nitric oxide determines the hypertensive effect of cell-free hemoglobin. Nat. Biotechnol. 16:672–76 [Google Scholar]
  130. Yu B, Raher MJ, Volpato GP, Bloch KD, Ichinose F, Zapol WM. 130.  2008. Inhaled nitric oxide enables artificial blood transfusion without hypertension. Circulation 117:1982–90 [Google Scholar]
  131. Yu B, Volpato GP, Chang K, Bloch KD, Zapol WM. 131.  2009. Prevention of the pulmonary vasoconstrictor effects of HBOC-201 in awake lambs by continuously breathing nitric oxide. Anesthesiology 110:113–22 [Google Scholar]
  132. Alayash AI. 132.  2004. Oxygen therapeutics: Can we tame haemoglobin?. Nat. Rev. Drug Discov. 3:152–59 [Google Scholar]
  133. Palmer AF. 133.  2006. Molecular volume and HBOC-induced vasoconstriction. Blood 108:3231–32 [Google Scholar]
  134. Chang TM. 134.  1998. Modified hemoglobin-based blood substitutes: crosslinked, recombinant and encapsulated hemoglobin. Vox Sang. 74:Suppl. 2233–41 [Google Scholar]
  135. Day TK. 135.  2003. Current development and use of hemoglobin-based oxygen-carrying (HBOC) solutions. J. Vet. Emerg. Crit. Care 13:77–93 [Google Scholar]
  136. Tsai AG, Cabrales P, Manjula BN, Acharya SA, Winslow RM, Intaglietta M. 136.  2006. Dissociation of local nitric oxide concentration and vasoconstriction in the presence of cell-free hemoglobin oxygen carriers. Blood 108:3603–10 [Google Scholar]
  137. Butt OI, Buehler PW, D'Agnillo F. 137.  2011. Blood-brain barrier disruption and oxidative stress in guinea pig after systemic exposure to modified cell-free hemoglobin. Am. J. Pathol. 178:1316–28 [Google Scholar]
  138. Butt OI, Buehler PW, D'Agnillo F. 138.  2010. Differential induction of renal heme oxygenase and ferritin in ascorbate and nonascorbate producing species transfused with modified cell-free hemoglobin. Antioxid. Redox Signal. 12:199–208 [Google Scholar]
  139. Rice J, Philbin N, Light R, Arnaud F, Steinbach T. 139.  et al. 2008. The effects of decreasing low-molecular weight hemoglobin components of hemoglobin-based oxygen carriers in swine with hemorrhagic shock. J. Trauma 64:1240–57 [Google Scholar]
  140. Kasper SM, Walter M, Grune F, Bischoff A, Erasmi H, Buzello W. 140.  1996. Effects of a hemoglobin-based oxygen carrier (HBOC-201) on hemodynamics and oxygen transport in patients undergoing preoperative hemodilution for elective abdominal aortic surgery. Anesth. Analg. 83:921–27 [Google Scholar]
  141. LaMuraglia GM, O'Hara PJ, Baker WH, Naslund TC, Norris EJ. 141.  et al. 2000. The reduction of the allogenic transfusion requirement in aortic surgery with a hemoglobin-based solution. J. Vasc. Surg. 31:299–308 [Google Scholar]
  142. Jahr JS, Mackenzie C, Pearce LB, Pitman A, Greenburg AG. 142.  2008. HBOC-201 as an alternative to blood transfusion: efficacy and safety evaluation in a multicenter phase III trial in elective orthopedic surgery. J. Trauma 64:1484–97 [Google Scholar]
  143. Freilich D, Pearce LB, Pitman A, Greenburg G, Berzins M. 143.  et al. 2009. HBOC-201 vasoactivity in a phase III clinical trial in orthopedic surgery subjects—extrapolation of potential risk for acute trauma trials. J. Trauma 66:365–76 [Google Scholar]
  144. Sehgal LR, Gould SA, Rosen AL, Sehgal HL, Moss GS. 144.  1984. Polymerized pyridoxylated hemoglobin: a red cell substitute with normal oxygen capacity. Surgery 95:433–38 [Google Scholar]
  145. Yu B, Shahid M, Egorina EM, Sovershaev MA, Raher MJ. 145.  et al. 2010. Endothelial dysfunction enhances vasoconstriction due to scavenging of nitric oxide by a hemoglobin-based oxygen carrier. Anesthesiology 112:586–94 [Google Scholar]
  146. Handrigan MT, Bentley TB, Oliver JD, Tabaku LS, Burge JR, Atkins JL. 146.  2005. Choice of fluid influences outcome in prolonged hypotensive resuscitation after hemorrhage in awake rats. Shock 23:337–43 [Google Scholar]
  147. Moore EE, Moore FA, Fabian TC, Bernard AC, Fulda GJ. 147.  et al. 2009. Human polymerized hemoglobin for the treatment of hemorrhagic shock when blood is unavailable: the USA multicenter trial. J. Am. Coll. Surg. 208:1–13 [Google Scholar]
  148. Kipnis K, King NM, Nelson RM. 148.  2006. Trials and errors: barriers to oversight of research conducted under the emergency research consent waiver. IRB: Ethics Hum. Res. 28:16–19 [Google Scholar]
  149. Adamson JG, Moore C. 149.  1998. Hemolink™, an o-raffinose crosslinked hemoglobin-based oxygen carrier. Blood Substitutes: Principles, Methods, Products, and Clinical Trials TMS Chang 62–81 Basel, Switz: Krager Landes Syst. [Google Scholar]
  150. Cheng DC, Mazer CD, Martineau R, Ralph-Edwards A, Karski J. 150.  et al. 2004. A phase II dose-response study of hemoglobin raffimer (Hemolink) in elective coronary artery bypass surgery. J. Thorac. Cardiovasc. Surg. 127:79–86 [Google Scholar]
  151. Greenburg AG, Kim HW. 151.  2004. Use of an oxygen therapeutic as an adjunct to intraoperative autologous donation to reduce transfusion requirements in patients undergoing coronary artery bypass graft surgery. J. Am. Coll. Surg. 198:373–85 [Google Scholar]
  152. Hill SE, Gottschalk LI, Grichnik K. 152.  2002. Safety and preliminary efficacy of hemoglobin raffimer for patients undergoing coronary artery bypass surgery. J. Cardiothorac. Vasc. Anesth. 16:695–702 [Google Scholar]
  153. Lieberthal W, Fuhro R, Freedman JE, Toolan G, Loscalzo J, Valeri CR. 153.  1999. O-raffinose cross-linking markedly reduces systemic and renal vasoconstrictor effects of unmodified human hemoglobin. J. Pharmacol. Exp. Ther. 288:1278–87 [Google Scholar]
  154. Matheson B, Kwansa HE, Bucci E, Rebel A, Koehler RC. 154.  2002. Vascular response to infusions of a nonextravasating hemoglobin polymer. J. Appl. Physiol. 93:1479–86 [Google Scholar]
  155. Bucci E, Kwansa H, Koehler RC, Matheson B. 155.  2007. Development of zero-link polymers of hemoglobin, which do not extravasate and do not induce pressure increases upon infusion. Artif. Cells Blood Substit. Immobil. Biotechnol. 35:11–18 [Google Scholar]
  156. Jia Y, Alayash AI. 156.  2009. Effects of cross-linking and zero-link polymerization on oxygen transport and redox chemistry of bovine hemoglobin. Biochim. Biophys. Acta 1794:1234–42 [Google Scholar]
  157. Cabrales P, Zhou Y, Harris DR, Palmer AF. 157.  2010. Tissue oxygenation after exchange transfusion with ultrahigh-molecular-weight tense- and relaxed-state polymerized bovine hemoglobins. Am. J. Physiol. Heart Circ. Physiol. 298:H1062–71 [Google Scholar]
  158. Baek JH, Zhou Y, Harris DR, Schaer DJ, Palmer AF, Buehler PW. 158.  2012. Down selection of polymerized bovine hemoglobins for use as oxygen releasing therapeutics in a guinea pig model. Toxicol. Sci. Off. J. Soc. Toxicol. 127:567–81 [Google Scholar]
  159. Palmer AF, Sun G, Harris DR. 159.  2009. The quaternary structure of tetrameric hemoglobin regulates the oxygen affinity of polymerized hemoglobin. Biotechnol. Prog. 25:1803–9 [Google Scholar]
  160. Buehler PW, Zhou Y, Cabrales P, Jia Y, Sun G. 160.  et al. 2010. Synthesis, biophysical properties and pharmacokinetics of ultrahigh molecular weight tense and relaxed state polymerized bovine hemoglobins. Biomaterials 31:3723–35 [Google Scholar]
  161. Zhou Y, Jia Y, Buehler PW, Chen G, Cabrales P, Palmer AF. 161.  2011. Synthesis, biophysical properties, and oxygenation potential of variable molecular weight glutaraldehyde-polymerized bovine hemoglobins with low and high oxygen affinity. Biotechnol. Prog. 27:1172–84 [Google Scholar]
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