Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress 2023 EHA Congress 2023 ASCO Annual Meeting
Clinical Collections
Advances in Alzheimer’s

At a glance: The ONWARDS insulin icodec trials

A round-up of the ONWARDS phase 3 clinical trials evaluating the novel weekly insulin icodec in people with diabetes.
ADVANCED SEARCH
Log in
Top
Thrombosis Journal
Published in: Thrombosis Journal 1/2014

Open Access 01-12-2014 | Review

Hypothermia: effects on platelet function and hemostasis

Authors: Sven Van Poucke, Kris Stevens, Abraham Emanuel Marcus, Marcus Lancé

Published in: Thrombosis Journal | Issue 1/2014

Login to get access

Abstract

Mild therapeutic hypothermia is considered standard care in the treatment of patients resuscitated from cardiac arrest. With increasingly more frequent concomitant use of platelet-inhibiting drugs, clinicians must be cognizant of the ramifications of hypothermia on platelet function as part of hemostasis. The effects of hypothermia on platelet function have been studied for more than 50 years, but the results are inconsistent and may be related to the circumstances during which hypothermia is achieved. This review summarizes current knowledge of platelet function during hypothermia and the impact on hemostasis.
Literature
1.
Field CL, Tablin F: Response of Northern Elephant Seal platelets to pressure and temperature changes: a comparison with human platelets. Comp Biochem Physiol A Mol Integr Physiol. 2012, 162: 289-295. 10.1016/j.cbpa.2012.01.023.CrossRefPubMed
2.
Hurd PL, van Anders SM: Latitude, digit ratios, and Allen’s and Bergmann’s rules: a comment on Loehlin, McFadden, Medland, and Martin (2006). Arch Sex Behav. 2007, 36: 139-141. 10.1007/s10508-006-9149-9. author reply 143CrossRefPubMed
3.
Cooper ST, Richters KE, Melin TE, Liu Z, Hordyk PJ, Benrud RR, Geiser LR, Cash SE, Shelley CS, Howard DR, Ereth MH, Sola-Visner MC: The hibernating 13-lined ground squirrel as a model organism for potential cold storage of platelets. Am J Physiol Regul Integr Comp Physiol. 2012, 302: R1202-R1208. 10.1152/ajpregu.00018.2012.PubMedCentralCrossRefPubMed
4.
5.
Lee S, Alston T: A little hypothermia goes a long way. Crit Care Med. 2012, 40: 1369-1370. 10.1097/CCM.0b013e31823b8b6a.CrossRefPubMed
6.
Díaz M, Becker DE: Thermoregulation: physiological and clinical considerations during sedation and general anesthesia. Anesth Prog. 2010, 57: 25-32. 10.2344/0003-3006-57.1.25. quiz 33–4PubMedCentralCrossRefPubMed
7.
8.
Horosz B, Malec-Milewska M: Inadvertent intraoperative hypothermia. Anaesthesiol Intensive Ther. 2013, 45: 38-43. 10.5603/AIT.2013.0009.CrossRefPubMed
9.
Bratincsák A, Palkovits M: Activation of brain areas in rat following warm and cold ambient exposure. Neuroscience. 2004, 127: 385-397. 10.1016/j.neuroscience.2004.05.016.CrossRefPubMed
10.
Kurz A: Physiology of thermoregulation. Best Pract Res Clin Anaesthesiol. 2008, 22: 627-644. 10.1016/j.bpa.2008.06.004.CrossRefPubMed
11.
Schwertz H, Rowley JW, Tolley ND, Campbell RA, Weyrich AS: Assessing protein synthesis by platelets. Methods Mol Biol. 2012, 788: 141-153. 10.1007/978-1-61779-307-3_11. [Methods in Molecular Biology]CrossRefPubMed
12.
Jenne CN, Urrutia R, Kubes P: Platelets: bridging hemostasis, inflammation, and immunity. Int J Lab Hematol. 2013, 35: 254-261. 10.1111/ijlh.12084.CrossRefPubMed
13.
Horstman LL, Jy W, Ahn YS, Zivadinov R, Maghzi AH, Etemadifar M, Steven Alexander J, Minagar A: Role of platelets in neuroinflammation: a wide-angle perspective. J Neuroinflammation. 2010, 7: 10-10.1186/1742-2094-7-10.PubMedCentralCrossRefPubMed
14.
Jurk K, Kehrel BE: Platelets: physiology and biochemistry. Semin Thromb Hemost. 2005, 31: 381-392. 10.1055/s-2005-916671.CrossRefPubMed
15.
Gawaz M: Intelligent platelet inhibitors are on the horizon. Arterioscler Thromb Vasc Biol. 2011, 31: 1949-1950. 10.1161/ATVBAHA.111.232173.CrossRefPubMed
16.
Topcic D, Kim W, Holien JK, Jia F, Armstrong PC, Hohmann JD, Straub A, Krippner G, Haller CA, Domeij H, Hagemeyer CE, Parker MW, Chaikof EL, Peter K: An activation-specific platelet inhibitor that can be turned on/off by medically used hypothermia. Arter Thromb Vasc Biol. 2011, 31: 2015-2023. 10.1161/ATVBAHA.111.226241.CrossRef
17.
Han HS, Park J, Kim J-H, Suk K: Molecular and cellular pathways as a target of therapeutic hypothermia: pharmacological aspect. Curr Neuropharmacol. 2012, 10: 80-87. 10.2174/157015912799362751.PubMedCentralCrossRefPubMed
18.
Hall R, Mazer CD: Antiplatelet drugs: a review of their pharmacology and management in the perioperative period. Anesth Analg. 2011, 112: 292-318. 10.1213/ANE.0b013e318203f38d.CrossRefPubMed
19.
Johansson BW: Drugs affect and are affected by body temperature. Lakartidningen. 2001, 98: 2178-2181.PubMed
20.
Mackowiak PA, Wasserman SS, Levine MM: A critical appraisal of 98.6°F, the upper limit of the normal body temperature, and other legacies of Carl Reinhold August Wunderlich. JAMA. 1992, 268: 1578-1580. 10.1001/jama.1992.03490120092034.CrossRefPubMed
21.
Krajewski S, Kurz J, Geisler T, Peter K, Wendel HP, Straub A: Combined blockade of ADP receptors and PI3-kinase p110beta fully prevents platelet and leukocyte activation during hypothermic extracorporeal circulation. PLoS One. 2012, 7: e38455-10.1371/journal.pone.0038455.PubMedCentralCrossRefPubMed
22.
Marx J: Rosen’s emergency medicine: concepts and clinical practice. Mosby/Elsevier; 2006:2239.
23.
Fröbert O, Christensen K, Fahlman A, Brunberg S, Josefsson J, Särndahl E, Swenson JE, Arnemo JM: Platelet function in brown bear (Ursus arctos) compared to man. Thromb J. 2010, 8: 11-10.1186/1477-9560-8-11.PubMedCentralCrossRefPubMed
24.
Storey KB: Out cold: biochemical regulation of mammalian hibernation - a mini-review. Gerontology. 2010, 56: 220-230. 10.1159/000228829.CrossRefPubMed
25.
Morrison JJ, Ross JD, Poon H, Midwinter MJ, Jansen JO: Intra-operative correction of acidosis, coagulopathy and hypothermia in combat casualties with severe haemorrhagic shock. Anaesthesia. 2013, 68: 846-850. 10.1111/anae.12316.CrossRefPubMed
26.
Mohr J, Ruchholtz S, Hildebrand F, Flohé S, Frink M, Witte I, Weuster M, Fröhlich M, van Griensven M, Keibl C, Mommsen P: Induced hypothermia does not impair coagulation system in a swine multiple trauma model. J Trauma Acute Care Surg. 2013, 74: 1014-1020. 10.1097/TA.0b013e3182826edd.CrossRefPubMed
27.
Kheirbek T, Kochanek AR, Alam HB: Hypothermia in bleeding trauma: a friend or a foe?. Scand J Trauma Resusc Emerg Med. 2009, 17: 1-15. 10.1186/1757-7241-17-65.CrossRef
28.
Meex I, Dens J, Jans F, Boer W, Vanhengel K, Vundelinckx G, Heylen R, De Deyne C: Cerebral tissue oxygen saturation during therapeutic hypothermia in post-cardiac arrest patients. Resuscitation. 2013, 84: 788-793. 10.1016/j.resuscitation.2013.01.003.CrossRefPubMed
29.
Absalom AR, Scheeren TWL: NIRS during therapeutic hypothermia: cool or hot?. Resuscitation. 2013, 2013: 95-96.
30.
Frink M, Flohé S, Van Griensven M, Mommsen P, Hildebrand F: Facts and fiction: the impact of hypothermia on molecular mechanisms following major challenge. Mediat Inflamm. 2012, 2012: 762840-CrossRef
31.
Broessner G, Fisher M, Schubert G, Metzler B, Schmutzhard E: Update on therapeutic temperature management. Crit Care. 2012, 16 (Suppl 2): 1-42.
32.
Palmiere C, Bardy D, Letovanec I, Mangin P, Augsburger M, Ventura F, Iglesias K, Werner D: Biochemical markers of fatal hypothermia. Forensic Sci Int. 2013, 226: 54-61. 10.1016/j.forsciint.2012.12.007.CrossRefPubMed
33.
Brändström H, Eriksson A, Giesbrecht G, Angquist K-A, Haney M: Fatal hypothermia: an analysis from a sub-arctic region. Int J Circumpolar Health. 2012, 71: 1-7. 10.3402/ijch.v71i0.18502.CrossRefPubMed
34.
Escalda A, Marques M, Silva-Carvalho L, Barradas MA, Silva-Carvalho J, Cruz JM, Mikhailidis DP: Hypothermia-induced haemostatic and biochemical phenomena. An experimental model. Platelets. 1993, 4: 17-22. 10.3109/09537109309013191.CrossRefPubMed
35.
Heni M, Saur SJ: Blood clotting at room temperature in cold agglutinin disease. Blood. 2013, 121: 4975-4975. 10.1182/blood-2012-12-472324.CrossRefPubMed
36.
Penela D, Magaldi M, Fontanals J, Martin V, Regueiro A, Ortiz JT, Bosch X, Sabaté M, Heras M: Hypothermia in acute coronary syndrome: brain salvage versus stent thrombosis?. J Am Coll Cardiol. 2013, 61: 686-687. 10.1016/j.jacc.2012.10.029.CrossRefPubMed
37.
38.
Andrews RK, Berndt MC: Platelet physiology: in cold blood. Curr Biol. 2003, 13: R282-R284. 10.1016/S0960-9822(03)00202-1.CrossRefPubMed
39.
Winokur R, Hartwig JH: Mechanism of shape change in chilled human platelets. Blood. 1995, 85: 1796-1804.PubMed
40.
Kawakami H, Higashihara M, Ohsaka M, Miyazaki K, Ikebe M, Hirano H: Myosin light chain phosphorylation is correlated with cold-induced changes in platelet shape. J Smooth Muscle Res. 2001, 37: 113-122. 10.1540/jsmr.37.113.CrossRefPubMed
41.
Broos K, Feys HB, De Meyer SF, Vanhoorelbeke K, Deckmyn H: Platelets at work in primary hemostasis. Blood Rev. 2011, 25: 155-167. 10.1016/j.blre.2011.03.002.CrossRefPubMed
42.
Grabowski EF, Yam K, Gerace M: Evaluation of hemostasis in flowing blood. Am J Hematol. 2012, 87 (Suppl 1): S51-S55. 10.1002/ajh.23207.CrossRefPubMed
43.
Baskurt OK, Meiselman HJ: Blood rheology and hemodynamics. Semin Thromb Hemost. 2003, 29: 435-450. 10.1055/s-2003-44551.CrossRefPubMed
44.
Zhang J, Wood J, Bergeron AL, McBride L, Ball C, Yu Q, Pusiteri AE, Holcomb JB, Dong J: Effects of low temperature on shear-induced platelet aggregation and activation. J Trauma Inj Infect Crit Care. 2004, 57: 216-223. 10.1097/01.TA.0000093366.98819.FE.CrossRef
45.
Egidi MG, D’Alessandro A, Mandarello G, Zolla L: Troubleshooting in platelet storage temperature and new perspectives through proteomics. Blood Transfus. 2010, 8 (Suppl 3): s73-s81.PubMedCentralPubMed
46.
Hessel EA, Schmer G, Dillard DH: Kinetics during Deep Hypothermia. J Surg Res. 1980, 34: 23-34. 10.1016/0022-4804(80)90078-5.CrossRef
47.
Hoffmeister KM, Felbinger TW, Denis V, Bergmeier W, Mayadas TN, Von Andrian UH, Wagner DD, Stossel TP, Hartwig JH: The clearance mechanism of chilled blood platelets Brigham and women’ s hospital. Cell. 2003, 112: 87-97. 10.1016/S0092-8674(02)01253-9.CrossRefPubMed
48.
Ao H, Moon JK, Tashiro M, Terasaki H: Delayed platelet dysfunction in prolonged induced canine hypothermia. Resuscitation. 2001, 51: 83-90. 10.1016/S0300-9572(01)00380-X.CrossRefPubMed
49.
De Vrij EL, Vogelaar PC, Goris M, Houwertjes MC, Herwig A, Dugbartey GJ, Boerema AS, Strijkstra AM, Bouma HR, Henning RH: Platelet dynamics during natural and pharmacologically induced torpor and forced hypothermia. PLoS One. 2014, 9: e93218-10.1371/journal.pone.0093218.PubMedCentralCrossRefPubMed
50.
Tanaka KA, Key NS, Levy JH: Blood coagulation: hemostasis and thrombin regulation. Anesth Analg. 2009, 108: 1433-1446. 10.1213/ane.0b013e31819bcc9c.CrossRefPubMed
51.
Lenting PJ, Casari C, Christophe OD, Denis CV: von Willebrand factor: the old, the new and the unknown. J Thromb Haemost. 2012, 10: 2428-2437. 10.1111/jth.12008.CrossRefPubMed
52.
Ai X, Gu Y: The effect of low temperature on von Willbrand factor expression of cultured human umbilical vein endothelial cells. Chin J Surg. 1997, 35: 597-599.PubMed
53.
Perutelli P, Amato S, Molinari AC: Cleavage of von Willebrand factor by ADAMTS-13 in vitro: effect of temperature and barium ions on the proteolysis kinetics. Blood Coagul Fibrinolysis. 2005, 16: 607-611. 10.1097/01.mbc.0000187251.32630.1f.CrossRefPubMed
54.
Carter T, Mashanov G, Ogden D, Zupančič G, Hannah MJ, Hewlett L, Knipe L: Temperature-dependence of weibel-palade body exocytosis and cell surface dispersal of von Willebrand factor and its propolypeptide. PLoS One. 2011, 6: e27314-10.1371/journal.pone.0019177.PubMedCentralCrossRefPubMed
55.
Dimitrov JD, Christophe OD, Kang J, Repessé Y, Delignat S, Kaveri SV, Lacroix-Desmazes S: Thermodynamic analysis of the interaction of factor VIII with von Willebrand factor. Biochemistry. 2012, 51: 4108-4116. 10.1021/bi300232d.CrossRefPubMed
56.
Lindenblatt N, Menger MD, Klar E, Vollmar B: Sustained hypothermia accelerates microvascular thrombus formation in mice. Am J Physiol Heart Circ Physiol. 2005, 289: H2680-H2687. 10.1152/ajpheart.00425.2005.CrossRefPubMed
57.
Berger G, Hartwell DW, Wagner DD: P-Selectin and platelet clearance. Blood. 1998, 92: 4446-4452.PubMed
58.
Michelson AD, MacGregor H, Barnard MR, Kestin AS, Rohrer MJ, Valeri CR: Reversible inhibition of human platelet activation by hypothermia in vivo and in vitro. Thromb Haemost. 1994, 71: 633-640.PubMed
59.
Faraday N, Rosenfeld B: In vitro hypothermia enhances platelet GPIIb-IIIa activation and P-selectin expression. Anesthesiology. 1998, 88: 1579-1585. 10.1097/00000542-199806000-00022.CrossRefPubMed
60.
Scharbert G, Kalb ML, Essmeister R, Kozek-Langenecker SA: Mild and moderate hypothermia increases platelet aggregation induced by various agonists: a whole blood in vitro study. Platelets. 2010, 21: 44-48. 10.3109/09537100903420269.CrossRefPubMed
61.
Frelinger AL, Furman MI, Barnard MR, Krueger LA, Dae MW, Michelson AD: Combined effects of mild hypothermia and glycoprotein IIb/IIIa antagonists on platelet-platelet and leukocyte-platelet aggregation. Am J Cardiol. 2003, 92: 1099-1101. 10.1016/j.amjcard.2003.06.007.CrossRefPubMed
62.
Högberg C, Erlinge D, Braun OÖ: Mild hypothermia does not attenuate platelet aggregation and may even increase ADP-stimulated platelet aggregation after clopidogrel treatment. Thromb J. 2009, 7: 2-10.1186/1477-9560-7-2.PubMedCentralCrossRefPubMed
63.
Lantz N, Hechler B, Ravanat C, Cazenave J-P, Gachet C: A high concentration of ADP induces weak platelet granule secretion independently of aggregation and thromboxane A2 production. Thromb Haemost. 2007, 98: 1145-1147.PubMed
64.
Xavier RG, White AE, Fox SC, Wilcox RG, Heptinstall S: Enhanced platelet aggregation and activation under conditions of hypothermia. Thromb Haemost. 2007, 98: 1266-1275.PubMed
65.
Straub A, Krajewski S, Hohmann JD, Westein E, Jia F, Bassler N, Selan C, Kurz J, Wendel HP, Dezfouli S, Yuan Y, Nandurkar H, Jackson S, Hickey MJ, Peter K: Evidence of platelet activation at medically used hypothermia and mechanistic data indicating ADP as a key mediator and therapeutic target. Arter Thromb Vasc Biol. 2011, 31: 1607-1616. 10.1161/ATVBAHA.111.226373.CrossRef
66.
Scharbert G, Kalb M, Marschalek C, Kozek-Langenecker SA: The effects of test temperature and storage temperature on platelet aggregation: a whole blood in vitro study. Anesth Analg. 2006, 102: 1280-1284. 10.1213/01.ane.0000199399.04496.6d.CrossRefPubMed
67.
Wang X: Comparative analysis of various platelet glycoprotein IIb/IIIa antagonists on shear-induced platelet activation and adhesion. Blood. 2002, 100: 61B-
68.
Wolberg AS, Meng ZH, Monroe DM, Hoffman M: A systematic evaluation of the effect of temperature on coagulation enzyme activity and platelet function. J Trauma Inj Infect Crit Care. 2004, 56: 1221-1228. 10.1097/01.TA.0000064328.97941.FC.CrossRef
69.
Wallin BG: Neural control of human skin blood flow. J Auton Nerv Syst. 1990, 30 (Suppl): S185-S190. 10.1016/0165-1838(90)90128-6.CrossRefPubMed
70.
Evora PRB, Cable DG, Chua YL, Rodrigues AJ, Pearson PJ, Schaff HV: Nitric oxide and prostacyclin-dependent pathways involvement on in vitro induced hypothermia. Cryobiology. 2007, 54: 106-113. 10.1016/j.cryobiol.2006.12.002.CrossRefPubMed
71.
Gyulkhandanyan AV, Mutlu A, Freedman J, Leytin V: Selective triggering of platelet apoptosis, platelet activation or both. Br J Haematol. 2013, 161: 245-254. 10.1111/bjh.12237.CrossRefPubMed
72.
van der Wal DE, Du VX, Lo KSL, Rasmussen JT, Verhoef S, Akkerman JWN: Platelet apoptosis by cold-induced glycoprotein Ibα clustering. J Thromb Haemost. 2010, 8 (11): 2554-2562. 10.1111/j.1538-7836.2010.04043.x.CrossRefPubMed
Metadata
Title
Hypothermia: effects on platelet function and hemostasis
Authors
Sven Van Poucke
Kris Stevens
Abraham Emanuel Marcus
Marcus Lancé
Publication date
01-12-2014
Publisher
BioMed Central
Published in
Thrombosis Journal / Issue 1/2014
Electronic ISSN: 1477-9560
DOI
https://doi.org/10.1186/s12959-014-0031-z

Other articles of this Issue 1/2014

Thrombosis Journal 1/2014 Go to the issue

Original basic research

Rivaroxaban versus enoxaparin/vitamin K antagonist therapy in patients with venous thromboembolism and renal impairment

Original clinical investigation

Incidence of venous thromboembolism in northern Sweden (VEINS): a population-based study

Original clinical investigation

The influence of Erythropoietin on platelet activation, thrombin generation and FVII/active FVII in patients with AMI

Original clinical investigation

The effect of a continuing medical education program on Venous thromboembolism prophylaxis utilization and mortality in a tertiary-care hospital

Original clinical investigation

Risk of venous thromboembolic disease and adequacy of prophylaxis in hospitalized patients in Argentina: a multicentric cross-sectional study

Original clinical investigation

Simple and rapid assay for effect of the new oral anticoagulant (NOAC) rivaroxaban: preliminary results support further tests with all NOACs

ACC 2024 Congress Coverage

Heart Failure Video

Year in Review: Heart failure and cardiomyopathies

Watch now

Watch this official video from ACC.24. Dr. Biykem Bozkurt discuss last year's major advances in heart failure and cardiomyopathies.

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

16-04-2024 Type 2 Diabetes News

Incentivised to exercise

11-04-2024 Lifestyle Modifications News

New intervention for STEMI-related cardiogenic shock

10-04-2024 Myocardial Infarction News

» View more highlights on the ACC 2024 congress hub page

Image Credits