The effects of temperature on micro-rheological variables have not been completely revealed yet.
OBJECTIVE:
To investigate micro-rheological effects of heat treatment in human, rat, dog, and porcine blood samples.
METHODS:
Red blood cell (RBC) - buffer suspensions were prepared and immersed in a 37, 40, and 43°C heat-controlled water bath for 10 minutes. Deformability, as well as mechanical stability of RBCs were measured in ektacytometer. These tests were also examined in whole blood samples at various temperatures, gradually between 37 and 45°C in the ektacytometer.
RESULTS:
RBC deformability significantly worsened in the samples treated at 40 and 43°C, more expressed in human, porcine, rat, and in smaller degree in canine samples. The way of heating (incubation vs. ektacytometer temperation) and the composition of the sample (RBC-PBS suspension or whole blood) resulted in the different magnitude of RBC deformability deterioration. Heating affected RBC membrane (mechanical) stability, showing controversial alterations.
CONCLUSION:
Significant changes occur in RBC deformability by increasing temperature, showing inter-species differences. The magnitude of alterations is depending on the way of heating and the composition of the sample. The results may contribute to better understanding the micro-rheological deterioration in hyperthermia or fever.
MackowiakPA. Temperature regulation and pathogenesis of fever. Mandell, Douglas and Bennett’s Principles and Practise of Infectious Disease, Vol. 1, 6th edition. Elsevier Churchill Livingstone; 2005. pp. 703-18.
2.
DinarelloCA, GelfandJA. Fever and hyperthermia. In: Fauci AS, Kasper DL, Longo DL, Braunwald E, Hauser SL, Jameson JL, Loscalzo J, editor. Harrison’s Principles of Internal Medicine. McGraw-Hill’s Company, 17th edition; 2005. pp. 90-4.
3.
GomezCR. Disorders of body temperature. Handb Clin Neurol. 2014;120:947–57. doi: 10.1016/B978-0-7020-4087-0.00062-0
4.
CheshireWPJr. Thermoregulatory disorders and illness related to heat and cold stress. Auton Neurosci. 2016;196:91–104. doi: 10.1016/j.autneu.2016.01.001
5.
HasdayJD, SinghIS. Fever and the heat shock response: distinct, partially overlapping processes. Cell Stress Chaperones. 2000;5(5):471–80. doi: 10.1379/1466-1268(2000)005<0471:fathsr>2.0.co;2
6.
LimCL, ByrneC, LeeJK. Human thermoregulation and measurement of body temperature in exercise and clinical settings. Ann Acad Med Singa. 2008;37(4):347–53.
7.
BlatteisCM. The onset of fever: new insights into its mechanism. Prog Brain Res. 2007;162:3–14. doi: 10.1016/S0079-6123(06)62001-3
8.
RomanovskyAA. Thermoregulation: some concepts have changed. Functional architecture of the thermoregulatory system. Am J Physiol Regul Integr Comp Physiol. 2007;292(1):R37–46. doi: 10.1152/ajpregu.00668.2006
9.
JungF, Krüger-GengeA, FrankeRP, HufertF, KüpperJH. COVID-19 and the endothelium. Clin Hemorheol Microcirc. 2020;75(1):7–11. doi: 10.3233/CH-209007
10.
RenouxC, FortR, NaderE, BoissonC, JolyP, StaufferE, et al. Impact of COVID-19 on red blood cell rheology. Br J Haematol. 2021 Jan 7. doi: 10.1111/bjh.17306. Epub ahead of print.
11.
HamTH, ShenSC. Studies on the destruction of red blood cells; thermal injury; action of heat in causing increased spheroidicity, osmotic and mechanical fragilities and hemolysis of erythrocytes; observations on the mechanisms of destruction of such erythrocytes in dogs and in a patient with a fatal thermal burn. Blood. 1948;3(4):373–403.
12.
RakowAL, HochmuthRM. Effect of heat treatment on the elasticity of human erythrocyte membrane. Biophys J. 1975;15(11):1095–100.
13.
BaskurtOK, HardemanMR, UyukluM, UlkerP, CengizM, NemethN, et al.Comparison of three commercially available ektacytometers with different shearing geometries. Biorheology. 2009;46(3):251–64. doi: 10.3233/BIR-2009-0536
14.
WindbergerU, BaskurtOK. Comparative hemorheology. In: Handbook of Hemorheology and Hemodynamics. Baskurt OK, Hardeman MR, Rampling MW, Meiselman HJ, editors. Amsterdam: IOS Press; 2007. pp. 267-285.
15.
NemethN, SogorV, KissF, UlkerP. Interspecies diversity of erythrocyte mechanical stability at various combinations in magnitude and duration of shear stress, and osmolality. Clin Hemorheol Microcirc. 2016;63(4):381–398. doi: 10.3233/CH-152031
16.
HardemanMR, GoedhartPT, ShinS. Methods in hemorheology. In: Handbook of Hemorheology and Hemodynamics. Baskurt OK, Hardeman MR, Rampling MW, Meiselman HJ, editors. Amsterdam: IOS Press; 2007. pp. 242-266.
17.
BaskurtOK, HardemanMR, UyukluM, UlkerP, CengizM, NemethN, ShinS, AlexyT, MeiselmanHJ. Parameterization of red blood cell elongation index–shear stress curves obtained by ektacytometry. Scand J Clin Lab Invest. 2009;69(7):777–88. doi: 10.3109/00365510903266069
18.
LarcanA, LambertH, Laprevote-HeullyMC, AlexandreP, SimonM. Heat stroke and disseminated intravascular coagulation. Apropos of 2 cases. Sem Ho. 1978;54(17-20):603–19.
19.
KarnaukhN, FilipchenkoL, Koval’chukT, BilykL, LevinaE. Morphologic changes due to hyperthermia (experimental study). Meditsina Truda i Promyshlennaia Ekologiia. 2004. pp. 17-20.
20.
VladM, IonescuN, IspasAT, GiuvărăşteanuI, UngureanuE, StoicaC. Morphological changes during acute experimental short-term hyperthermia. Rom J Morphol Embryol. 2010;51(4):739–44.
21.
WalterEJ, Hanna-JummaS, CarrarettoM, ForniL. The pathophysiological basis and consequences of fever. Crit Care. 2016;20(1):200.
22.
LapshaVI, GurinVN. Changes in the ultrastructure of histohematic barrier in the rat right atrium after short-term and prolonged heat stress. Morfologiia. 2006;129(1):49–53.
23.
SinghM, StoltzJF. Influence of temperature variation from 5 degrees C to 37 degrees C on aggregation and deformability of erythrocytes. Clin Hemorheol Microcirc. 2002;26(1):1–7.
24.
EvansEA, HochmuthRM. Mechanochemical properties of membranes. In: Bronner F, Kleinzeller A. Current Topics in Membranes and Transport. Academic Press; 1978. pp. 1-64.
25.
ChasisJA, ShohetSB. Red cell biochemical anatomy and membrane properties. Annu Rev Physiol. 1987;49, 237–48.
26.
LipowskyHH. Microvascular rheology and hemodynamics. Microcirculation. 2005;12(1):5–15. doi: 10.1080/10739680590894966
27.
NemethN, DeakA, SzentkeresztyZ, PetoK. Effects and influencing factors on hemorheological variables taken into consideration in surgical pathophysiology research. Clin Hemorheol Microcirc. 2018;69(1-2):133–140. doi: 10.3233/CH-189105
28.
BaskurtOK, MatF. Importance of measurement temperature in detecting the alterations of red blood cell aggregation and deformability studied by ektacytometry: a study on experimental sepsis in rats. Clin Hemorheol Microcirc. 2000;23(1):43–9.
29.
LecklinT, EggintonS, NashGB. Effect of temperature on the resistance of individual red blood cells to flow through capillary-sized apertures. Pflugers Arch. 1996;432(5):753–9. doi: 10.1007/s004240050195
30.
UyukluM, CengizM, UlkerP, HeverT, TripetteJ, ConnesP, et al.Effects of storage duration and temperature of human blood on red cell deformability and aggregation. Clin Hemorheol Microcirc. 2009;41(4):269–78. doi: 10.3233/CH-2009-1178
31.
ArtmannGM, KelemenCh, PorstD, BüldtG, ChienS. Temperature transitions of protein properties in human red blood cells. Biophys J. 1998;75(6):3179–83. doi: 10.1016/S0006-3495(98)77759-8
32.
GershfeldNL, MurayamaM. Thermal instability of red blood cell membrane bilayers: temperature dependence of hemolysis. J Membr Biol. 1988;101(1):67–72. doi: 10.1007/BF01872821
33.
SimmondsMJ, DetterichJA, ConnesP. Nitric oxide, vasodilation and the red blood cell. Biorheology. 2014;51(2-3):121–34. doi: 10.3233/BIR-140653
34.
YalcinO, UlkerP, YavuzerU, MeiselmanHJ, BaskurtOK. Nitric oxide generation by endothelial cells exposed to shear stress in glass tubes perfused with red blood cell suspensions: role of aggregation. Am J Physiol Heart Circ Physiol. 2008;294(5):H2098–105. doi: 10.1152/ajpheart.00015.2008
35.
BouchardJN, YamasakiH. Heat stress stimulates nitric oxide production in Symbiodinium microadriaticum: A possible linkage between nitric oxide and the coral bleaching phenomenon. Plant Cell Physiol. 2008;49(4):641–52. doi: 10.1093/pcp/pcn037
BernardC, MervalR, EspositoB, TedguiA. Elevated temperature accelerates and amplifies the induction of nitric oxide synthesis in rat macrophages. Eur J Pharmacol. 1994;270(1):115–8. doi: 10.1016/0926-6917(94)90087-6
38.
GerstbergerR. Nitric oxide and body temperature control. News Physiol Sci. 1999;14:30–6. doi: 10.1152/physiologyonline.1999.14.1.30
39.
HakimTS, PedotoA, NandiJ, BoscoG, RubiniA, MangarD, et al.Hypothermia attenuates NO production in anesthetized rats with endotoxemia. Naunyn Schmiedebergs Arch Pharmacol. 2014;387(7):659–65. doi: 10.1007/s00210-014-0977-1
