Abstract
Background
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.
Methods
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.
Results
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 %).
Conclusion
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.
Similar content being viewed by others
References
Mertens I, Van Gaal LF (2002) Obesity, haemostasis, and the fibrinolytic system. Obes Rev 3:85–101
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 168:1678–1683
De Pergola G, Panncciulli N (2002) Coagulation and fibrinolysis abnormalities in obesity. J Endocrinol Invest 25:899–904
Faber DR, de Groot G, Visseren FLJ (2009) Role of adipose tissue in haemostasis, coagulation, and fibrinolysis. Obes Rev 10:554–563
Santilli F, Vazzana N, Liani R, Guagnano MT, Davi G (2012) Platelet activation in obesity and metabolic syndrome. Obes Rev 13:27–42
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 220:215–218
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 30:2639–2647
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 113:383–391
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 13:819–825
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 15:1368–1374
Prystowsky JB, Morasch MD, Escandari MK, Hungness ES, Nagle AP (2005) Prospective analysis of the incidence of deep venous thrombosis in bariatric surgery. Surgery 138:759–765
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 194:709–711
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 208:917–923
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 18:1082–1084
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 22:158–166
Furie B, Furie BL (2008) Mechanism of thrombus formation. N Eng J Med 359:938–949
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 92:572–577
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 146:764–772
Luddington RJ (2005) Thrombelastography/thromboelastometry. Clin Lab Haematol 27:81–90
Sorensen B, Johansen P, Christiansen K, Woelke M, Ingerslev J (2003) Whole-blood coagulation thrombelastographic profiles employing minimal tissue factor activation. J Thromb Haemost 1:551–558
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 3:2039–2043
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 94:113–118
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 120:1640–1645
Gonzalez E, Kashuk JL, Moore EE, Silliman CC (2010) Differentiation of enzymatic from platelet hypercoagulability using the novel thrombelastography parameter delta (∆). J Surg Res 163:96–101
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–e34
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 9:1236–1245
Livingston EH (2012) Pitfalls in using BMI as a selection criterion for bariatric surgery. Curr Opin Endocrinol Diabetes Obes 19:347–351
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 22:2384–2391
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 19:98–104
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 125:1768–1775
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 22:56–61
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 19:1278–1285
McCrath DJ, Cerboni E, Frumento RJ, Hirsh AL, Bennett-Guerrero E (2005) Thromboelastography maximum amplitude predicts postoperative thrombotic complications including myocardial infarction. Anesth Analg 100:1576–1583
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 21:256–261
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 22:113–118
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 7:14–21
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 125:220–223
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 4:625–631
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 3:494–495
Disclosures
Pilar Taura, Eva Rivas, Graciela Martinez-Palli, Annabel Blasi, Juan Carlos Holguera, Jaume Balust, Salvadora Delgado, and Antonio M. Lacy has no conflicts of interest or financial ties to disclose.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Taura, P., Rivas, E., Martinez-Palli, G. et al. Clinical markers of the hypercoagulable state by rotational thrombelastometry in obese patients submitted to bariatric surgery. Surg Endosc 28, 543–551 (2014). https://doi.org/10.1007/s00464-013-3203-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00464-013-3203-1