Abstract
Purpose
We assessed the impact of completing the Hotter’n Hell Hundred (HHH), an annual 164 km road cycling event performed in a hot environment, on hemostatic balance in men.
Methods
Sixteen men who completed the ride in <6 h were included in this study. Plasma samples were collected on that morning of the ride (PRE) and immediately on the completion of the ride (IP). Primary hemostasis was assessed by platelet count and von Willebrand factor antigen (vWF:Ag). Coagulation was assessed by measuring prothrombin fragment 1 + 2 (PTF 1 + 2) and thrombin-antithrombin complex (TAT), whereas fibrinolysis was assessed by plasminogen activator inhibitor antigen (PAI-1 Ag), tissue plasminogen activator (tPA Ag), and D-Dimer analyses.
Results
Compared to PRE, increases (p < 0.001) were observed at IP for platelets (39 %), vWF:Ag (65 %), PTF 1 + 2 (47 %), TAT (81 %), tPA Ag (231 %), PAI-1 Ag (148 %), and D-Dimer (54 %). PRE PAI-1 Ag concentrations were directly related to BMI and waist circumference (p < 0.05). D-Dimer concentrations at IP correlated positively with age (p < 0.05).
Conclusions
Completing the HHH activated the coagulation and fibrinolytic systems in balance. Age was positively correlated with IP D-Dimer concentrations. Additionally, participants displaying a larger BMI and waist circumference exhibited a positive correlation with PRE PAI-1 Ag concentrations.
Similar content being viewed by others
Abbreviations
- BMI:
-
Body mass index
- CVD:
-
Cardiovascular disease
- DVT:
-
Deep vein thrombosis
- HHH:
-
Hotter’N Hell Hundred
- IP:
-
Immediate post-ride
- PAI-1 Ag:
-
Plasminogen activator inhibitor-1
- PRE:
-
Pre-ride
- PTF 1 + 2:
-
Prothrombin fragment 1 + 2
- PE:
-
Pulmonary embolism
- TAT:
-
Thrombin-antithrombin complex
- tPA:
-
Tissue plasminogen activator
- vWF:Ag:
-
von Willebrand factor antigen
References
Arai M, Yorfuji H, Ikematsu S, Nagasawa H, Fujimaki M, Fukutake K, Katsumura T, Ishii T, Iwane H (1990) Influences of strenuous exercise (triathalon) on blood coagulation and fibrinolytic system. Thromb Res 57:465–471
Armstrong LE, Casa DJ, Emmanuel H, Ganio MS, Klau JF, Lee EC, Maresh CM, McDermott BP, Stearns RL, Vingren JL, Wingo JE, Williamson KH, Yamamoto LM (2012) Nutritional, physiological, and perceptual responses during a summer ultraendurance cycling event. J Strength Cond Res 26:307–318
Bartsch P, Welsch B, Albert M, Friedmann B, Levi M, Kruithof EK (1995) Balanced activation of coagulation and fibrinolysis after a 2-h triathlon. Med Sci Sports Exerc 27:1465–1470
Bedrak E, Beer G, Furman KI (1964) Fibrinolytic activity and muscular exercise in heat. J Appl Physiol 19:469–471
Belalcazar LM, Ballantyne CM, Lang W, Haffner SM, Rushing J, Schwenke DC, Pi-Sunyer FX, Tracy RP (2011) Metabolic factors, adipose tissue, and plasminogen activator inhibitor-1 levels in type 2 diabetes: findings from the look AHEAD study. Arter Thromb Vasc Biol 31:1689–1695
Boldt LH, Fraszl W, Röcker L, Schefold JC, Steinach M, Noack T, Gunga HC (2008) Changes in the haemostatic system after thermoneutral and hyperthermic water immersion. Eur J Appl Physiol 102:547–554
Bouchama A, Bridey F, Hammami MM, Lacombe C, al-Shali E, al-Ohali Y, Combe F, al-Sedairy S, de Prost D (1996) Activation of coagulation and fibrinolysis in heatstroke. Thromb Haemost 76:909–915
Bouchama A, Al-Mohanna F, Assad L, Baturcam E, Eldali A, Owaidah T, Dehbi M (2012) Tissue factor/factor VIIa pathway mediates coagulation activation in induced-heat stroke in the baboon. Crit Care Med 40:1229–1236
Delp MD, O’Leary DS (1985) Integrative control of the skeletal muscle microcirculation in the maintenance of arterial pressure during exercise. J Appl Physiol 97:1112–1118
Dimitriadou C, Dessypris A, Louizou C, Mandalaki T (1997) Marathon run II: effects on platelet aggregation. Thromb Haemost 37:451–455
Dufaux B, Order U, Liesen H (1991) Effect of a short maximal physical exercise on coagulation, fibrinolysis, and complement system. Int J Sports Med 1:S38–S42
Go AS, Mozaffarian D, Roger VL, Benjamin EJ, Berry JD, Blaha MJ, Dai S, Ford ES, Fox CS, Franco S, Fullerton HJ, Gillespie C, Hailpern SM, Heit JA, Howard VJ, Huffman MD, Judd SE, Kissela BM, Kittner SJ, Lackland DT, Lichtman JH, Lisabeth LD, Mackey RH, Magid DJ, Marcus GM, Marelli A, Matchar DB, McGuire DK, Mohler ER, Moy CS, Mussolino ME, Neumar RW, Nichol G, Pandey DK, Paynter NP, Reeves MJ, Sorlie PD, Stein J, Towfighi A, Turan TN, Virani SS, Wong ND, Woo D, Turner MB (2014) Heart disease and stroke statistics–2014 update: a report from the American Heart Association. Circulation 129:e28–e292
Gough SC, Whitworth S, Rice PJ, Grant PJ (1992) The effect of exercise and heart rate on fibrinolytic activity. Blood Coagul Fibrinol 3:179–182
Hanke AA, Staib A, Gorlinger K, Perrey M, Dirkmann D, Kienbaum P (2010) Whole blood coagulation and platelet activation in the athlete: a comparison of marathon, triathalon and long distance cycling. Eur J Med Res 15:559–565
Herren T, Bartsch P, Haeberli A, Straub PW (1992) Increased thrombin-antithrombin III complexes after 1 h of physical exercise. J Appl Physiol 73:2499–2504
Hilberg T, Glaser D, Reckhart C, Prasa D, Stuzebecher J, Gabriel HH (2003) Blood coagulation and fibrinolysis after long-duration exercise controlled by individual anaerobic threshold. Eur J Appl Physiol 90:639–642
Holst AG, Jensen G, Prescott E (2010) Risk factors for venous thromboembolism: results from the Copenhagen City Heart Study. Circulation 121:1896–1903
Hostler D, Suyama J, Guyette FX, Moore CG, Pryor RR, Khorana P, McEntire SJ, Comer D, Reis SE (2014) A randomized control trial of aspirin and exertion in thermal protective clothing. Prehosp Emerg Care 18:359–367
Huck V, Schneider MF, Gorzelanny C, Schneider SW (2014) The various states of von Willebrand factor and their function in physiology and pathophysiology. Thromb Haemost 111:598–609
Knudaen JB, Brodthagen U, Gormsen J, Jordal R, Norregaard-Hansen K, Paulex PE (1982) Platelet function and fibrinolytic activity during distance running. Scand J Haematol 29:425–430
Kupchak BR, Volk BM, Kunces LJ, Kraemer WJ, Hoffman MD, Phinney SD, Volek JS (2013) Alterations in coagulatory and fibrinolytic systems following an ultra-marathon. Eur J Appl Physiol 113:2705–2712
Kvernmo HD, Osterud B (1997) The effect of physical conditioning suggests adaptation in procoagulant and fibrinolytic potential. Thromb Res 87:559–569
Larsson PT, Wallen NH, Egberg N, Hjemdahl P (1992) Alpha-adrenoceptor blockade by phentolamine inhibits adrenaline-induced platelet activation in vivo without affecting resting measurements. Clin Sci (Lond) 82:369–376
Leon AS (2000) Exercise following myocardial infarction. Current recommendations. Sports Med 29:301–311
Levi M, van der Poll T, Schultz M (2012) Infection and Inflammation as risk factors for thrombosis and atherosclerosis. Semin Thromb Hemost 38:506–514
Levin EG, Marzec U, Anderson J, Harker LA (1984) Thrombin stimulates tissue plasminogen activator release from cultured human endothelial cells. J Clin Invest 74:1988–1995
Levin EG, Santell L, Saljooque F (1993) Hyperosmotic stress stimulates tissue plasminogen activator expression by a PKC-independent pathway. Am J Physiol 265:C387–C396
Lohman TG, Roche AF, Mortorell R (1988) Anthropometrics standardization reference manual. Human Kinetics Books, Champaign, IL, pp 55–70
Mandalaki T, Dessypris A, Louizou C, Bossinakou I, Panayotopoulou C, Antonopoulou A (1977) Marathon run I: effects on blood coagulation and fibrinolysis. Thromb Haemost 37:444–450
Meka N, Katragadda S, Cherian B, Arora RR (2008) Endurance exercise and resistance training in cardiovascular disease. Ther Adv Cardiovasc Dis 2:115–121
Meyer M, Ostrowski SR, Overgaad A, Ganio MS, Secher NH, Crandall CG, Johansson PI (2013) Hypercoagulability in response to elevated body temperature and central hypovolemia. J Surg Res 185:e93–e100
Michalska M, Iwan-Zietek I, Gnilka W, Dabrowiecki S, Goralczyk B, Goralczyk K, Drela E, Rosc D (2013) PAI-1 and α2-AP in patients with morbid obesity. Adv Clin Exp Med 22:801–807
Mockel M, Ulrich NV, Heller G Jr, Rocker L, Hansen R, Riess H, Patscheke H, Stork T, Frei U, Ruf A (2001) Platelet activation through triathalon competition in ultra-endurance trained athletes: impact of thrombin and plasmin generation and catecholamine release. Int J Sports Med 22:337–343
Parker BA, Augeri AL, Capizzi JA, Ballard KD, Kupchak BR, Volek JS, Troyanos C, Kriz P, D’Hemecourt P, Thompson PD (2012) Effect of marathon run and air travel on pre- and post-run soluble d-dimer, microparticle procoagulant activity, and p-selectin levels. Am J Cardiol 109(10):1521–1525
Pinsky DJ (1996) Hypoxia-induced exocytosis of endothelial cell Weibel-Palade bodies. A mechanism for rapid neutrophil recruitment after cardiac preservation. J Clin Invest 97:493–500
Prisco D, Paniccia R, Bandinelli B, Fedi S, Cellai AP, Liotta AA, Gatteschi L, Giusti B, Colella A, Abbate R, Gensini GF (1998) Evaluation of clotting and fibrinolytic activation after protracted physical exercise. Thromb Res 89:73–78
Roberts GT, Ghebeh H, Chishti MA, Al-Mohanna F, El-Sayed R, Al-Mohanna F, Bouchama A (2008) Microvascular injury, thrombosis, inflammation, and apoptosis in the pathogenesis of heatstroke: a study in the baboon model. Arterioscler Thromb Vasc Biol 28:1130–1136
Rock G, Tittley P, Pipe A (1997) Coagulation factor changes following endurance exercise. Clin J Sports Med 7:94–99
Rocker L, Taenzer M, Drygas WK, Lill H, Heyduck B, Altenkirch HU (1990) Effect of prolonged physical exercise on the fibrinolytic system. Eur J Appl Physiol Occup Physiol 60:478–481
Rocker L, Mockel M, Westpfal KP, Gunga HC (1996) Influence of maximal ergometric exercise on endothelin concentrations in relation to molecular markers of hemostatic system. Thromb Haemost 75:612–616
Sacco RL, Adams R, Albers G, Alberts MJ, Benavente O, Furie K, Goldstein LB, Gorelick P, Halperin J, Harbaugh R, Johnston CS, Katzan I, Kelly-Hayes M, Kenton EJ, Marks M, Schwamm LH, Tomsick T (2006) Guidelines for prevention of stroke in patients with ischemic stroke or transient ischemic attack: a statement for healthcare professionals from the American Heart Association/American Stroke Association on stroke: co-sponsored by the Council on Cardiovascular Radiology and Intervention. Circulation 113:e409–e449
Sadler JE (1998) Biochemistry and genetics of von Willebrand factor. Annul Rev Biochem 67:395–424
Schobersberger W, Wirleitner B, Puschendorf B, Koller A, Villiger B, Frey W, Mair J (1996) Influence of an ultramarathon race at moderate altitude on coagulation and fibrinolysis. Fibrinolysis 10:37–42
Shimomura I, Funahashi T, Takahashi M, Maeda K, Kotani K, Nakamura T, Yamashita S, Miura M, Fukuda Y, Takemura K, Tokunaga K, Matsuzawa Y (1996) Enhanced expression of PAI-1 in visceral fat: possible contributor to vascular disease in obesity. Natl Med 2:800–803
Smith DL, Petruzzello SJ, Goldstein E, Ahmad U, Tangella K, Freud GG, Horn GP (2011) Effect of live-fire training drills on firefighters’ platelet number and function. Prehosp Emerg Care 15:233–239
Spiel AO (2008) Von Willebrand factor in cardiovascular disease: focus on acute coronary syndromes. Circulation 117:1449–1459
Sporn LA, Marder VJ, Wagner DD (1986) Inducible secretion of large, biologically potent von Willebrand factor multimers. Cell 146:185–190
Strother SV, Bull JM, Branham SA (1986) Activation of coagulation during therapeutic whole body hyperthermia. Thromb Res 43:353–360
Sumann G, Fries D, Griesmacher A, Falkensammer G, Klingler A, Koller A, Streif W, Greie S, Schobersberger B, Schobersberger W (2007) Blood coagulation activation and fibrinolysis during a downhill marathon run. Blood Coagul Fibrinol 18:435–440
Tabet JY, Meurin P, Driss AB, Weber H, Renaud N, Grosdemouge A, Beauvais F, Cohen-Solal A (2009) Benefits of exercise training in chronic heart failure. Arch Cardiovasc Dis 102:721–730
Tamura K, Kubota K, Kurabayashi H, Shirakura T (1996) Effects of hyperthermia stress on fibrinolytic system. Int J Hyperthermia 12:31–36
Thogersen AM, Jansson JH, Boman K, Nilaaon TK, Weinehall L, Huhtasaari F, Hallmans G (1998) High plasminogen activator inhibitor and tissue plasminogen activator levels in plasma precede a first acute myocardial infarction in both men and women: evidence for the fibrinolytic system as an independent primary risk factor. Circulation 98:2241–2247
van Loon BJ, Heere LP, Kluft C, Briet E, Dooijewaard G, Meinders AE (1992) Fibrinolytic system during long-distance running in IDDM patients and in healthy subjects. Diabetes Care 15:991–996
Verhovsek M, Douketis JD, Yi Q, Shrivastava S, Tait RC, Baglin T, Poli D, Lim W (2008) Systematic review: D-dimer to predict recurrent disease after stopping anticoagulant therapy for unprovoked venous thromboembolism. Ann Intern Med 149:481–490
Wang JS, Li YS, Chen JC, Chen YW (2005) Effects of exercise training and deconditioning on platelet aggregation induced by alternating sheer stress in men. Arterioscler Thromb Vasc Biol 25:454–460
Wells PS (2005) The role of qualitative D-dimer assays, clinical probability, and noninvasive imaging tests for the diagnosis of deep vein thrombosis and pulmonary embolism. Semin Vasc Med 5:340–350
Zhu GJ, Abbadini M, Donati MB, Mussoni L (1989) Tissue-type plasminogen activator release in response to epinephrine in perfused rat hindlegs. Am J Physiol 256:H404–H410
Acknowledgments
The authors gratefully acknowledge the expertise Keith H Williamson, MD (medical director) for his expertise and the HHH Expo committee for the use of facilities in the Wichita Falls Multi Purpose Event Center. This research study was not funded by external sources; all funds were internal to the University of Connecticut or University of North Texas.
Conflict of interest
The authors declare that they have no conflict of interest.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Narihiko Kondo.
Rights and permissions
About this article
Cite this article
Kupchak, B.R., McKenzie, A.L., Luk, HY. et al. Effect of cycling in the heat for 164 km on procoagulant and fibrinolytic parameters. Eur J Appl Physiol 115, 1295–1303 (2015). https://doi.org/10.1007/s00421-015-3107-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00421-015-3107-y