Influence of red blood cell aggregation on perfusion of an artificial microvascular network

Microcirculation

Volumn 24, Issue 5, 2017, Pages

  Reinhart, Walter H ^a   Piety, Nathaniel Z ^b   Shevkoplyas, Sergey S ^b  

^a KANTONSSPITAL GRAUBÜNDEN   (Switzerland)

^b UNIVERSITY OF HOUSTON   (United States)

Author keywords

artificial microvascular network; dextran; hematocrit; microvascular perfusion; red blood cell aggregation

Indexed keywords

DEXTRAN; OXYGEN;

ARTERIOLE; ARTICLE; CAPILLARY; CELL SUSPENSION; CONTROLLED STUDY; ERYTHROCYTE; ERYTHROCYTE ADHESIVENESS; ERYTHROCYTE AGGREGATION; FLOW RATE; HEMATOCRIT; HUMAN; HUMAN CELL; PERFUSION; PRIORITY JOURNAL; VENULE; VISCOSITY; BIOLOGICAL MODEL; BLOOD VISCOSITY; METABOLISM; MICROVASCULATURE; PHYSIOLOGY;

BLOOD VISCOSITY; ERYTHROCYTE AGGREGATION; HEMATOCRIT; HUMANS; MICROVESSELS; MODELS, CARDIOVASCULAR; OXYGEN; PERFUSION;

EID: 85022023320     PISSN: 10739688     EISSN: 15498719     Source Type: Journal    
DOI: 10.1111/micc.12317     Document Type: Article

References (73)

1. Baskurt OK, Hardeman MR, Rampling MW, Meiselman HJ. Handbook of Hemorheology and Hemodynamics. Amsterdam: IOS Press; 2007.
2. Ami RB, Barshtein G, Zeltser D et al. Parameters of red blood cell aggregation as correlates of the inflammatory state. Am J Physiol Heart Circ Physiol. 2001;280:H1982–H1988.
3. Goldin Y, Tulshinski T, Arbel Y et al. Rheological consequences of acute infections: the rheodifference between viral and bacterial infections. Clin Hemorheol Micro. 2007;36:111–119.
4. Alt E, Amann-Vesti BR, Madl C, Funk G, Koppensteiner R. Platelet aggregation and blood rheology in severe sepsis/septic shock: relation to the sepsis-related organ failure assessment (SOFA) score. Clin Hemorheol Micro. 2004;30:107–115.
5. Lee BK, Durairaj A, Mehra A, Wenby RB, Meiselman HJ, Alexy T. Hemorheological abnormalities in stable angina and acute coronary syndromes. Clin Hemorheol Micro. 2008;39:43–51.
6. Zorio E, Murado J, Arizo D et al. Haemorheological parameters in young patients with acute myocardial infarction. Clin Hemorheol Micro. 2008;39:33–41.
7. Tikhomirova IA, Oslyakova AO, Mikhailova SG. Microcirculation and blood rheology in patients with cerebrovascular disorders. Clin Hemorheol Micro. 2011;49:295–305.
8. Koscielny J, Jung EM, Mrowietz C, Kiesewetter H, Latza R. Blood fluidity, fibrinogen, and cardiovascular risk factors of occlusive arterial disease: results of the Aachen study. Clin Hemorheol Micro. 2004;31:185–195.
9. Cicco G, Pirrelli A. Red blood cell (RBC) deformability, RBC aggregability and tissue oxygenation in hypertension. Clin Hemorheol Micro. 1999;21:169–177.
10. Zilberman-Kravits D, Harman-Boehm I, Shuster T, Meyerstein N. Increased red cell aggregation is correlated with HbA1C and lipid levels in type 1 but not type 2 diabetes. Clin Hemorheol Micro. 2006;35:463–471.
11. Toker S, Rogowski O, Melamed S et al. Association of components of the metabolic syndrome with the appearance of aggregated red blood cells in the peripheral blood. An unfavorable hemorheological finding. Diabetes/Metab Res Rev. 2005;21:197–202.
12. Kwaan HC. Role of plasma proteins in whole blood viscosity: a brief clinical review. Clin Hemorheol Micro. 2010;44:167–176.
13. Spengler MI, Svetaz MJ, Leroux MB et al. Erythrocyte aggregation in patients with systemic lupus erythematosus. Clin Hemorheol Micro. 2011;47:279–285.
14. Vaya A, Calvo J, Alcala C, Mico L, Todoli J, Ricart JM. Rheological alterations and thrombotic events in patients with systemic lupus erythematosus. Clin Hemorheol Micro. 2012;51:51–58.
15. Flormann D, Kuder E, Lipp P, Wagner C, Kaestner L. Is there a role of C-reactive protein in red blood cell aggregation? Int J Lab Hematol. 2015;37:474–482.
16. Gabay C, Kushner I. Acute-phase proteins and other systemic responses to inflammation. N Engl J Med. 1999;340:448–454.
17. Koenig W. Fibrin(ogen) in cardiovascular disease: an update. Thromb Haemost. 2003;89:601–609.
18. Baskurt OK, Temiz A, Meiselman HJ. Red blood cell aggregation in experimental sepsis. J Lab Clin Med. 1997;130:183–190.
19. Fabry TL. Mechanism of erythrocyte aggregation and sedimentation. Blood. 1987;70:1572–1576.
20. Katanov D, Gompper G, Fedosov DA. Microvascular blood flow resistance: role of red blood cell migration and dispersion. Microvasc Res. 2015;99:57–66.
21. Yaylali YT, Susam I, Demir E et al. Increased red blood cell deformability and decreased aggregation as potential adaptive mechanisms in the slow coronary flow phenomenon. Coron Artery Dis. 2013;24:11–15.
22. Arbel Y, Banai S, Benhorin J et al. Erythrocyte aggregation as a cause of slow flow in patients of acute coronary syndromes. Int J Cardiol. 2012;154:322–327.
23. Tripette J, Alexy T, Hardy-Dessources MD et al. Red blood cell aggregation, aggregate strength and oxygen transport potential of blood are abnormal in both homozygous sickle cell anemia and sickle-hemoglobin C disease. Haematologica. 2009;94:1060–1065.
24. Vicaut E. Opposite effects of red blood cell aggregation on resistance to blood flow. J Cardiovasc Surg (Torino). 1995;36:361–368.
25. Charansonney O, Mouren S, Dufaux J, Duvelleroy M, Vicaut E. Red blood cell aggregation and blood viscosity in an isolated heart preparation. Biorheology. 1993;30:75–84.
26. Jung F, Mrowietz C, Hiebl B, Franke RP, Pindur G, Sternitzky R. Influence of rheological parameters on the velocity of erythrocytes passing nailfold capillaries in humans. Clin Hemorheol Micro. 2011;48:129–139.
27. Chien S, Usami S, Dellenback RJ, Gregersen MI, Nanninga LB, Guest MM. Blood viscosity: influence of erythrocyte aggregation. Science. 1967;157:829–831.
28. Ong PK, Jain S, Namgung B, Woo YI, Kim S. Cell-free layer formation in small arterioles at pathological levels of erythrocyte aggregation. Microcirculation. 2011;18:541–551.
29. Suzuki Y, Tateishi N, Soutani M, Maeda N. Flow behavior of erythrocytes in microvessels and glass capillaries: effects of erythrocyte deformation and erythrocyte aggregation. Int J Microcirc Clin Exp. 1996;16:187–194.
30. Barras JP. Blood rheology - general review. Bibl Haematol. 1969;33:277–297.
31. Nash G, Wenby R, Sowemimocoker S, Meiselman H. Influence of cellular properties on red-cell aggregation. Clin Hemorheology. 1987;7:93–108.
32. Burns JM, Yang X, Forouzan O, Sosa JM, Shevkoplyas SS. Artificial microvascular network: a new tool for measuring rheologic properties of stored red blood cells. Transfusion. 2012;52:1010–1023.
33. Forouzan O, Yang X, Sosa JM, Burns JM, Shevkoplyas SS. Spontaneous oscillations of capillary blood flow in artificial microvascular networks. Microvasc Res. 2012;84:123–132.
34. Reinhart WH, Piety NZ, Deuel JW et al. Washing stored red blood cells in an albumin solution improves their morphologic and hemorheologic properties. Transfusion. 2015;55:1872–1881.
35. Reinhart WH, Piety NZ, Goede JS, Shevkoplyas SS. Effect of osmolality on erythrocyte rheology and perfusion of an artificial microvascular network. Microvasc Res. 2015;98:102–107.
36. Shevkoplyas SS, Gifford SC, Yoshida T, Bitensky MW. Prototype of an in vitro model of the microcirculation. Microvasc Res. 2003;65:132–136.
37. Shevkoplyas SS, Yoshida T, Gifford SC, Bitensky MW. Direct measurement of the impact of impaired erythrocyte deformability on microvascular network perfusion in a microfluidic device. Lab Chip. 2006;6:914–920.
38. Surgenor DMN. The Red Blood Cell, 2nd edn. New York, Academic Press, 1974.
39. Chong-Martinez B, Buchanan TA, Wenby RB, Meiselman HJ. Decreased red blood cell aggregation subsequent to improved glycaemic control in Type 2 diabetes mellitus. Diabet Med. 2003;20:301–306.
40. Rampling MW, Whittingstall P, Martin G et al. A comparison of the rheologic properties of neonatal and adult blood. Pediatr Res. 1989;25:457–460.
41. Razavian SM, Guillemin MT, Guillet R, Beuzard Y, Boynard M. Assessment of red blood cell aggregation with dextran by ultrasonic interferometry. Biorheology. 1991;28:89–97.
42. Sowemimo-Coker SO, Whittingstall P, Pietsch L, Bauersachs RM, Wenby RB, Meiselman HJ. Effects of cellular factors on the aggregation behavior of human, rat and bovine erythrocytes. Clinical Hemorheology. 1989;9:723–737.
43. Vicaut E, Hou X, Decuypere L, Taccoen A, Duvelleroy M. Red blood cell aggregation and microcirculation in rat cremaster muscle. Int J Microcirc Clin Exp. 1994;14:14–21.
44. Brust M, Aouane O, Thiebaud M et al. The plasma protein fibrinogen stabilizes clusters of red blood cells in microcapillary flows. Sci Rep. 2014;4:4348.
45. Kim S, Popel AS, Intaglietta M, Johnson PC. Aggregate formation of erythrocytes in postcapillary venules. Am J Physiol Heart Circ Physiol. 2005;288:H584–H590.
46. McHedlishvili G, Gobejishvili L, Beritashvili N. Effect of intensified red blood cell aggregability on arterial pressure and mesenteric microcirculation. Microvasc Res. 1993;45:233–242.
47. Baskurt OK, Bor-Kucukatay M, Yalcin O. The effect of red blood cell aggregation on blood flow resistance. Biorheology. 1999;36:447–452.
48. Braasch D. The missing negative effect of red cell aggregation upon blood flow in small capillaries at low shear forces. Biorheology Suppl. 1984;1:227–230.
49. 2 transport in small arterioles. Clin Hemorheol Micro. 2015;59:163–175.
50. Verkeste CM, Boekkooi PF, Saxena PR, Peeters LL. Increased red cell aggregation does not reduce uteroplacental blood flow in the awake, hemoconcentrated, late-pregnant guinea pig. Pediatr Res. 1992;31:91–93.
51. Yalcin O, Uyuklu M, Armstrong JK, Meiselman HJ, Baskurt OK. Graded alterations of RBC aggregation influence in vivo blood flow resistance. Am J Physiol Heart Circ Physiol. 2004;287:H2644–H2650.
52. Baskurt OK, Meiselman HJ. RBC aggregation: more important than RBC adhesion to endothelial cells as a determinant of in vivo blood flow in health and disease. Microcirculation. 2008;15:585–590.
53. Bishop JJ, Nance PR, Popel AS, Intaglietta M, Johnson PC. Effect of erythrocyte aggregation on velocity profiles in venules. Am J Physiol Heart Circ Physiol. 2001;280:H222–H236.
54. Tripette J, Nguyen LC, Allard L, Robillard P, Soulez G, Cloutier G. In vivo venous assessment of red blood cell aggregate sizes in diabetic patients with a quantitative cellular ultrasound imaging method: proof of concept. PLoS ONE. 2015;10:e0124712.
55. Reinhart WH, Lutolf O, Nydegger UR, Mahler F, Straub PW. Plasmapheresis for hyperviscosity syndrome in macroglobulinemia Waldenstrom and multiple myeloma: influence on blood rheology and the microcirculation. J Lab Clin Med. 1992;119:69–76.
56. Fahraeus R, Lindqvist T. The viscosity of blood in narrow capillary tubes. Am J Physiol. 1931;96:562–568.
57. Secomb TW, Pries AR, Gaehtgens P. Hematocrit fluctuations within capillary tubes and estimation of Fahraeus effect. Int J Microcirc Clin Exp. 1987;5:335–345.
58. Baskurt OK, Meiselman HJ. Erythrocyte aggregation: basic aspects and clinical importance. Clin Hemorheol Micro. 2013;53:23–37.
59. Burns JM, Yoshida T, Dumont LJ, Yang X, Piety NZ, Shevkoplyas SS. Deterioration of red blood cell mechanical properties is reduced in anaerobic storage. Blood Transfus 2016; 14: 80–88.
60. Piety NZ, Reinhart WH, Pourreau PH, Abidi R, Shevkoplyas SS. Shape matters: the effect of red blood cell shape on perfusion of an artificial microvascular network. Transfusion. 2016;56:844–851.
61. Hennerici MG, Kay R, Bogousslavsky J, Lenzi GL, Verstraete M, Orgogozo JM, investigators E. Intravenous ancrod for acute ischaemic stroke in the European Stroke Treatment with Ancrod Trial: a randomised controlled trial. Lancet 2006; 368: 1871–1878.
62. Levy DE, del Zoppo GJ, Demaerschalk BM et al. Ancrod in acute ischemic stroke: results of 500 subjects beginning treatment within 6 hours of stroke onset in the ancrod stroke program. Stroke. 2009;40:3796–3803.
63. Matsuda H, Shoemaker WC. Survivor's and nonsurvivors’ responses to dextran 40. Hemodynamic and oxygen transport changes in critically ill patients. Arch Surg. 1975;110:301–305.
64. Dubin A, Pozo MO, Casabella CA et al. Comparison of 6% hydroxyethyl starch 130/0.4 and saline solution for resuscitation of the microcirculation during the early goal-directed therapy of septic patients. J Crit Care. 2010;25(659):e651–e658.
65. Perner A, Haase N, Winkel P et al. Long-term outcomes in patients with severe sepsis randomised to resuscitation with hydroxyethyl starch 130/0.42 or Ringer's acetate. Intensive Care Med. 2014;40:927–934.
66. Morariu AM, Gu YJ, Huet RC, Siemons WA, Rakhorst G, Oeveren WV. Red blood cell aggregation during cardiopulmonary bypass: a pathogenic cofactor in endothelial cell activation? Eur J Cardiothorac Surg. 2004;26:939–946.
67. Karakala N, Raghunathan K, Shaw AD. Intravenous fluids in sepsis: what to use and what to avoid. Curr Opin Crit Care. 2013;19:537–543.
68. Mutter TC, Ruth CA, Dart AB. Hydroxyethyl starch (HES) versus other fluid therapies: effects on kidney function. Cochrane Database Syst Rev 2013;7:CD007594.
69. Qureshi SH, Rizvi SI, Patel NN, Murphy GJ. Meta-analysis of colloids versus crystalloids in critically ill, trauma and surgical patients. Br J Surg. 2016;103:14–26.
70. Rochwerg B, Alhazzani W, Sindi A et al. Fluids in S, Septic Shock G; Fluid resuscitation in sepsis: a systematic review and network meta-analysis. Ann Intern Med. 2014;161:347–355.
71. Tseng MY, Hutchinson PJ, Kirkpatrick PJ. Effects of fluid therapy following aneurysmal subarachnoid haemorrhage: a prospective clinical study. Br J Neurosurg. 2008;22:257–268.
72. Zhong JZ, Wei D, Pan HF et al. Colloid solutions for fluid resuscitation in patients with sepsis: systematic review of randomized controlled trials. J Emerg Med. 2013;45:485–495.
73. Pries AR, Neuhaus D, Gaehtgens P. Blood viscosity in tube flow: dependence on diameter and hematocrit. Am J Physiol. 1992;263:H1770–H1778.