Surgical Endoscopy

, Volume 28, Issue 2, pp 543–551

Clinical markers of the hypercoagulable state by rotational thrombelastometry in obese patients submitted to bariatric surgery

  • Pilar Taura
  • Eva Rivas
  • Graciela Martinez-Palli
  • Annabel Blasi
  • Juan Carlos Holguera
  • Jaume Balust
  • Salvadora Delgado
  • Antonio M. Lacy



Metabolic and inflammatory disturbances associated with obesity are considered important trigger factors for venous thromboembolism (VTE). Identification of clinical markers indicating a hypercoagulability state could define a group of high-risk patients in the surgical setting. This study aimed to identify these markers using rotational thrombelastometry (ROTEM) analysis, an established method for hemostasis testing that can detect hyperfunctional stages of the clotting process.


From June to December 2010, this study investigated 109 consecutive obese patients (28 women and 22 men, mean age 46 years, body mass index 46.6 ± 7 kg/m2) with no history of VTE who were candidates for bariatric surgery. Preoperative clinical and metabolic characteristics and ROTEM analysis were recorded. Hypercoagulable risk was defined when patients showed a clot strength (G) of ≥11 dynes/cm2.


Of the 109 patients, 20 (18 %) were hypercoagulable according to ROTEM analysis. Metabolic/inflammatory biomarkers such as leptin, C-reactive protein, fibrinogen levels, and platelet count were significantly higher in the high-risk patients. In the multivariate analysis, fibrinogen was an independent predictor of G ≥ 11 dynes/cm2 [odds ratio (OR) 2.92, 95 % confidence interval (CI) 1.80–5.21, p = 0.023]. After adjustment to other data, only waist circumference affected the prediction [OR 4.42, 95 % CI 2.27–6.71, p = 0.009]. Receiver operating characteristic curve analysis showed that 3.95 g/l was the best cutoff point for fibrinogen predictability (sensitivity 100 %, specificity 41 %).


A hypercoagulability state in obese patients is associated with central obesity and high fibrinogen levels, which should be considered clinical hallmarks of this state. More aggressive perioperative prophylaxis for VTE should be recommended when these hallmarks are present in obese patients.


Metabolic syndrome Obesity Thrombelastometry analysis Thrombophilia 


  1. 1.
    Mertens I, Van Gaal LF (2002) Obesity, haemostasis, and the fibrinolytic system. Obes Rev 3:85–101PubMedCrossRefGoogle Scholar
  2. 2.
    Eichinger S, Hron G, Bialonczyk C, Hirschl M, Minar E, Wagner O, Heinze G, Kyrle PA (2008) Overweight, obesity, and the risk of recurrent venous thromboembolism. Arch Inter Med 168:1678–1683CrossRefGoogle Scholar
  3. 3.
    De Pergola G, Panncciulli N (2002) Coagulation and fibrinolysis abnormalities in obesity. J Endocrinol Invest 25:899–904PubMedGoogle Scholar
  4. 4.
    Faber DR, de Groot G, Visseren FLJ (2009) Role of adipose tissue in haemostasis, coagulation, and fibrinolysis. Obes Rev 10:554–563PubMedCrossRefGoogle Scholar
  5. 5.
    Santilli F, Vazzana N, Liani R, Guagnano MT, Davi G (2012) Platelet activation in obesity and metabolic syndrome. Obes Rev 13:27–42PubMedCrossRefGoogle Scholar
  6. 6.
    Prüller F, Raggam RB, Posch V, Almer G, Truschnig-Wilders M, Horejsi R, Mollër R, Weghuber D, Ille R, Schnedl W (2012) Trunk-weighted obesity, cholesterol levels, and low-grade inflammation are main determinants for enhanced thrombin generation. Atherosclerosis 220:215–218PubMedCrossRefGoogle Scholar
  7. 7.
    Beijers HJ, Ferreira I, Spronk HM, Bravenboer B, Dekeer JM, Nijpels G, ten Cate H, Stehouwer CD (2010) Body composition as determinant of thrombin generation in plasma. The Hoorn study. Arterioscler Thromb Vasc Biol 30:2639–2647PubMedCrossRefGoogle Scholar
  8. 8.
    Peverill RE, Teede HJ, Malan E, Kotsopoulos D, Smolich JJ, McGrath BP (2007) Relationship of waist and hip circumference with coagulation and fibrinolysis in postmenopausal women. Clin Sci 113:383–391PubMedCrossRefGoogle Scholar
  9. 9.
    Sapala JA, Wood MH, Schuhknecht MP, Sapala MA (2003) Fatal pulmonary embolism after bariatric operations for morbid obesity: a 24-year retrospective analysis. Obes Surg 13:819–825PubMedCrossRefGoogle Scholar
  10. 10.
    Hamad GG, Choban PS (2005) Enoxaparin for thromboprophylaxis in morbidly obese patients undergoing bariatric surgery: findings of the prophylaxis against VTE outcomes in bariatric surgery patients receiving enoxaparin (PROBE) study. Obes Surg 15:1368–1374PubMedCrossRefGoogle Scholar
  11. 11.
    Prystowsky JB, Morasch MD, Escandari MK, Hungness ES, Nagle AP (2005) Prospective analysis of the incidence of deep venous thrombosis in bariatric surgery. Surgery 138:759–765PubMedCrossRefGoogle Scholar
  12. 12.
    Kothari SN, Lambert PJ, Mathiason MA (2007) Best Poster Award: a comparison of thromboembolic and bleeding events following laparoscopic gastric bypass in patients treated with prophylactic regimens of unfractionated heparin or enoxaparin. Am J Surg 194:709–711PubMedCrossRefGoogle Scholar
  13. 13.
    Clements RH, Yellumahanthi K, Ballem N, Wesley M, Bland KI (2009) Pharmacologic prophylaxis against venous thromboembolic complications is not mandatory for all laparoscopic Roux-en-Y gastric bypass procedures. J Am Coll Surg 208:917–923PubMedCrossRefGoogle Scholar
  14. 14.
    Gonzalez QH, Tishler DS, Plata-Muñoz JJ, Bondora A, Vickers SM, Leath T, Clements RH (2004) Incidence of clinically evident deep venous thrombosis after laparoscopic Roux-en-Y gastric bypass. Surg Endosc 18:1082–1084PubMedGoogle Scholar
  15. 15.
    Jacobsen HJ, Bergland A, Reader J, Gislason HG (2012) High-volume bariatric surgery in a single center: safety, quality, cost-efficacy and teaching aspects in 2,000 consecutive cases. Obes Surg 22:158–166PubMedCrossRefGoogle Scholar
  16. 16.
    Furie B, Furie BL (2008) Mechanism of thrombus formation. N Eng J Med 359:938–949CrossRefGoogle Scholar
  17. 17.
    Mahla E, Lang T, Vicenzi MN, Werkgartner G, Maier R, Probst C, Metzler H (2001) Thromboelastography for monitoring prolonged hypercoagulability after major abdominal surgery. Anesth Analg 92:572–577PubMedCrossRefGoogle Scholar
  18. 18.
    Kashuk JL, Moore EE, Sabel A, Barnett, Haenel J, Le T, Pezold M, Lawrence J, Biffl WL, Cothren CC, Johnson JL (2009) Rapid thrombelastography (r-TEG) identifies hypercoagulability and predicts thromboembolic events in surgical patients. Surgery 146:764–772PubMedCrossRefGoogle Scholar
  19. 19.
    Luddington RJ (2005) Thrombelastography/thromboelastometry. Clin Lab Haematol 27:81–90PubMedCrossRefGoogle Scholar
  20. 20.
    Sorensen B, Johansen P, Christiansen K, Woelke M, Ingerslev J (2003) Whole-blood coagulation thrombelastographic profiles employing minimal tissue factor activation. J Thromb Haemost 1:551–558PubMedCrossRefGoogle Scholar
  21. 21.
    Rivard GE, Brummel K, Mann KG, Fan L, Hofer A, Cohen E (2005) Evaluation of the profile of thrombin generation during the process of whole-blood clotting as assessed by thromboelastography. J Thromb Haemost 3:2039–2043PubMedCentralPubMedCrossRefGoogle Scholar
  22. 22.
    Johansson PI, Svendsen MS, Salado J, Bochsen L, Kristensen AT (2008) Investigation of the thrombin-generating capacity evaluated by thrombogram and clot formation evaluated by thromboelastography of platelets stored in the blood bank for up to 7 days. Vox Sang 94:113–118PubMedCrossRefGoogle Scholar
  23. 23.
    Alberti KG, Eckel RH, Alberti KG, Grundy SM, Zimmet PZ, Cleeman JL, Donato KA, Frucharty JC, James WP, Loria CM, Smith SC (2009) Harmonizing the metabolic syndrome: a joint interim statement of the International Diabetes Federation Task Force on Epidemiology and Prevention; National Heart, Lung, and Blood Institute; American Heart Association; World Heart Federation; International Atherosclerosis Society; and International Association for the Study of Obesity. Circulation 120:1640–1645PubMedCrossRefGoogle Scholar
  24. 24.
    Gonzalez E, Kashuk JL, Moore EE, Silliman CC (2010) Differentiation of enzymatic from platelet hypercoagulability using the novel thrombelastography parameter delta (∆). J Surg Res 163:96–101PubMedCrossRefGoogle Scholar
  25. 25.
    Lind L, Siegbahn A, Ingelsson E, Sundström J, Ärnlöv J (2011) A detailed cardiovascular characterization of obesity without the metabolic syndrome. Arterioscler Thromb Vasc Biol 31:e27–e34PubMedCrossRefGoogle Scholar
  26. 26.
    Hanzu FA, Palomo M, Kalko SG, Parrizas SM, Garaulet M, Escolar G, Gomis R, Diaz-Ricart M (2011) Translational evidence of endothelial damage in obese individuals: inflammatory and prothrombotic responses. J Thromb Haemost 9:1236–1245PubMedCrossRefGoogle Scholar
  27. 27.
    Livingston EH (2012) Pitfalls in using BMI as a selection criterion for bariatric surgery. Curr Opin Endocrinol Diabetes Obes 19:347–351PubMedCrossRefGoogle Scholar
  28. 28.
    Raftopoulos I, Martindale C (2008) The effect of extended postdischarge chemical thromboprophylaxis on venous thromboembolism rates after bariatric surgery: a prospective comparison trial. Surg Endosc 22:2384–2391PubMedCrossRefGoogle Scholar
  29. 29.
    Maruyama K, Morishita E, Sekiya A, Omote M, Kadono T, Asakura H, Hashimoto M, Kobayashi M, Nakatsumi Y, Takada S, Ohtake S (2012) Plasma levels of platelet-derived microparticles in patients with obstructive sleep apnea syndrome. J Atheroscler Thromb 19:98–104PubMedCrossRefGoogle Scholar
  30. 30.
    Hui DS, Ko FW, Fok JP, Chan MC, Li TS, Tomlinson B, Cheng G (2004) The effects of nasal continuous positive airway pressure on platelet activation in obstructive sleep apnea syndrome. Chest 125:1768–1775PubMedCrossRefGoogle Scholar
  31. 31.
    Hioki Y, Aoki N, Kawano K, Homori M, Hasumura Y, Yasumura T, Maki A, Yoshino H, Yanagisawa, Ishikawa K (2001) Acute effects of cigarette smoking on platelet-dependent thrombin generation. Am Heart J 22:56–61CrossRefGoogle Scholar
  32. 32.
    Overby DW, Kohn GP, Cahan MA, Galanko JA, Colton K, Moll S, Farrell TM (2009) Prevalence of thrombophilias in patients presenting for bariatric surgery. Obes Surg 19:1278–1285PubMedCrossRefGoogle Scholar
  33. 33.
    McCrath DJ, Cerboni E, Frumento RJ, Hirsh AL, Bennett-Guerrero E (2005) Thromboelastography maximum amplitude predicts postoperative thrombotic complications including myocardial infarction. Anesth Analg 100:1576–1583PubMedCrossRefGoogle Scholar
  34. 34.
    Schaden E, Schober A, Hacker S, Spiss C, Chiari A, Kozek-Langenecker S (2010) Determination of enoxaparin with rotational thrombelastometry using the prothrombinase-induced clotting time reagent. Blood Coagul Fibrinolysis 21:256–261PubMedCrossRefGoogle Scholar
  35. 35.
    Forfori F, Ferro B, Mancini B, Letizia R, Abramo A, Anselmino M, Di Salvo C, Giunta F (2012) Role of thrombolestagrophy in monitoring perioperative coagulation status and effect of thromboprophylaxis in bariatric surgery. Obes Surg 22:113–118PubMedCrossRefGoogle Scholar
  36. 36.
    Artang R, Frandsen NJ, Nielsen JD (2009) Application of basic and composite thrombelastography parameters in monitoring of the antithrombotic effect of the low-molecular-weight heparin dalteparin: an in vivo study. Thromb J 7:14–21PubMedCentralPubMedCrossRefGoogle Scholar
  37. 37.
    Rondina MT, Wheeler M, Rodgers G, Draper L, Pendleton C (2010) Weight-based dosing of enoxaparin for VTE prophylaxis in morbidly obese, medically-ill patients. Thromb Res 125:220–223PubMedCentralPubMedCrossRefGoogle Scholar
  38. 38.
    Borkgren-Okonek MJ, Hart RW, Pantano JE, Rantis PC, Guske PJ, Kane JM, Gordon N, Sambol NC (2008) Enoxaparin thromboprophylaxis in gastric bypass patients: extended duration, dose stratification, and antifactor Xa activity. Surg Obes Relat Dis 4:625–631PubMedCrossRefGoogle Scholar
  39. 39.
    Clinical Issues Committee of the American Society for Metabolic and Bariatric Surgery (2007) Prophylactic measures to reduce the risk of venous thromboembolism in bariatric surgery patients (SOARD). Surg Obes Relat Dis 3:494–495CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  • Pilar Taura
    • 1
  • Eva Rivas
    • 1
  • Graciela Martinez-Palli
    • 1
  • Annabel Blasi
    • 1
  • Juan Carlos Holguera
    • 1
  • Jaume Balust
    • 1
  • Salvadora Delgado
    • 2
  • Antonio M. Lacy
    • 2
  1. 1.Department of Anesthesiology, Institute of Digestive and Metabolic Diseases, Hospital ClinicUniversity of BarcelonaBarcelonaSpain
  2. 2.Department of Gastrointestinal Surgery, Institute of Digestive and Metabolic Diseases, Hospital ClinicUniversity of BarcelonaBarcelonaSpain

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