Neurocritical Care

, Volume 24, Issue 1, pp 47–60 | Cite as

Prophylaxis of Venous Thrombosis in Neurocritical Care Patients: An Evidence-Based Guideline: A Statement for Healthcare Professionals from the Neurocritical Care Society

  • Paul NyquistEmail author
  • Cynthia Bautista
  • Draga Jichici
  • Joseph Burns
  • Sanjeev Chhangani
  • Michele DeFilippis
  • Fernando D. Goldenberg
  • Keri Kim
  • Xi Liu-DeRyke
  • William Mack
  • Kim Meyer
Review Article


The risk of death from venous thromboembolism (VTE) is high in intensive care unit patients with neurological diagnoses. This is due to an increased risk of venous stasis secondary to paralysis as well as an increased prevalence of underlying pathologies that cause endothelial activation and create an increased risk of embolus formation. In many of these diseases, there is an associated risk from bleeding because of standard VTE prophylaxis. There is a paucity of prospective studies examining different VTE prophylaxis strategies in the neurologically ill. The lack of a solid evidentiary base has posed challenges for the establishment of consistent and evidence-based clinical practice standards. In response to this need for guidance, the Neurocritical Care Society set out to develop and evidence-based guideline using GRADE to safely reduce VTE and its associated complications.


Venous thrombus Stroke Subarachnoid hemorrhage Traumatic brain injury Intracranial hemorrhage Pulmonary embolus 



Venous thromboembolism


Deep venous thrombus


Pulmonary embolus


Neurological intensive care unit


Intensive care unit


Aneurysmal subarachnoid hemorrhage


Intracranial hemorrhage


Traumatic intracranial hemorrhage


Ischemic stroke


Traumatic brain Injury


Spinal cord injury


Unfractionated heparin


Low-molecular-weight heparin


Intermittent pneumatic compression


Compression stockings


Inferior venous-caval filter


Conflict of interest

All of the authors declare that they have no conflicts of interest.

Supplementary material

12028_2015_221_MOESM1_ESM.docx (224 kb)
Supplementary material 1 (DOCX 224 kb)


  1. 1.
    Goldhaber SZ. Evolving concepts in thrombolytic therapy for pulmonary embolism. Chest. 1992;101(4 Suppl):183S–5S.PubMedCrossRefGoogle Scholar
  2. 2.
    White RH. The epidemiology of venous thromboembolism. Circulation. 2003;107(23 Suppl 1):I4–8.PubMedGoogle Scholar
  3. 3.
    McRae S. Treatment options for venous thromboembolism: lessons learnt from clinical trials. Thromb J. 2014;12(1):27.PubMedCentralPubMedCrossRefGoogle Scholar
  4. 4.
    Deitelzweig SB, Johnson BH, Lin J, Schulman KL. Prevalence of clinical venous thromboembolism in the USA: current trends and future projections. Am J Hematol. 2011;86(2):217–20.PubMedCrossRefGoogle Scholar
  5. 5.
    Cohen AT, Agnelli G, Anderson FA, Arcelus JI, Bergqvist D, Brecht JG, et al. Venous thromboembolism (VTE) in Europe. The number of VTE events and associated morbidity and mortality. Thromb Haemost. 2007;98(4):756–64.PubMedGoogle Scholar
  6. 6.
    Patel R, Cook DJ, Meade MO, Griffith LE, Mehta G, Rocker GM, et al. Burden of illness in venous thromboembolism in critical care: a multicenter observational study. J Crit Care. 2005;20(4):341–7.PubMedCrossRefGoogle Scholar
  7. 7.
    Attia J, Ray JG, Cook DJ, Douketis J, Ginsberg JS, Geerts WH. Deep vein thrombosis and its prevention in critically ill adults. Arch Intern Med. 2001;161(10):1268–79.PubMedCrossRefGoogle Scholar
  8. 8.
    Rolston JD, Han SJ, Lau CY, Berger MS, Parsa AT. Frequency and predictors of complications in neurological surgery: national trends from 2006 to 2011. J Neurosurg. 2014;120(3):736–45.PubMedCrossRefGoogle Scholar
  9. 9.
    Kelly J, Rudd A, Lewis R, Hunt BJ. Venous thromboembolism after acute stroke. Stroke. 2001;32(1):262–7.PubMedCrossRefGoogle Scholar
  10. 10.
    Brandes AA, Scelzi E, Salmistraro G, Ermani M, Carollo C, Berti F, et al. Incidence of risk of thromboembolism during treatment high-grade gliomas: a prospective study. Eur J Cancer. 1997;33(10):1592–6.PubMedCrossRefGoogle Scholar
  11. 11.
    Dhami MS, Bona RD, Calogero JA, Hellman RM. Venous thromboembolism and high grade gliomas. Thromb Haemost. 1993;70(3):393–6.PubMedGoogle Scholar
  12. 12.
    Bleau N, Patenaude V, Abenhaim HA. Risk of Venous thromboembolic events in pregnant patients with autoimmune diseases: a population-based study. Clin Appl Thromb Hemost. 2014. doi: 10.1177/1076029614553023.PubMedGoogle Scholar
  13. 13.
    Elkind MS. Inflammatory mechanisms of stroke. Stroke. 2010;41(10 Suppl):S3–8.PubMedCentralPubMedCrossRefGoogle Scholar
  14. 14.
    Roger VL, Go AS, Lloyd-Jones DM, Benjamin EJ, Berry JD, Borden WB, et al. Executive summary: heart disease and stroke statistics–2012 update: a report from the American Heart Association. Circulation. 2012;125(1):188–97.PubMedCrossRefGoogle Scholar
  15. 15.
    Roger VL, Go AS, Lloyd-Jones DM, Benjamin EJ, Berry JD, Borden WB, et al. Heart disease and stroke statistics–2012 update: a report from the American Heart Association. Circulation. 2012;125(1):e2–220.PubMedCentralPubMedCrossRefGoogle Scholar
  16. 16.
    Roger VL, O’Donnell CJ. Population health, outcomes research, and prevention: example of the American Heart Association 2020 goals. Circ Cardiovasc Qual Outcomes. 2012;5(1):6–8.PubMedCentralPubMedCrossRefGoogle Scholar
  17. 17.
    Wijdicks EF, Scott JP. Pulmonary embolism associated with acute stroke. Mayo Clin Proc. 1997;72(4):297–300.PubMedCrossRefGoogle Scholar
  18. 18.
    Indredavik B, Rohweder G, Naalsund E, Lydersen S. Medical complications in a comprehensive stroke unit and an early supported discharge service. Stroke. 2008;39(2):414–20.PubMedCrossRefGoogle Scholar
  19. 19.
    Minino AM, Murphy SL, Xu J, Kochanek KD. Deaths: final data for 2008. Natl Vital Stat Rep. 2011;59(10):1–126.Google Scholar
  20. 20.
    Jauch EC, Saver JL, Adams HP Jr, Bruno A, Connors JJ, Demaerschalk BM, et al. Guidelines for the early management of patients with acute ischemic stroke: a guideline for healthcare professionals from the American Heart Association/American Stroke Association. Stroke. 2013;44(3):870–947.PubMedCrossRefGoogle Scholar
  21. 21.
    Guyatt GH, Akl EA, Crowther M, Gutterman DD, Schuunemann HJ, et al. Executive summary: antithrombotic therapy and prevention of thrombosis, 9th ed: American College of Chest Physicians evidence-based clinical practice guidelines. Chest. 2012;141(2 Suppl):7S–47S.PubMedCentralPubMedCrossRefGoogle Scholar
  22. 22.
    Sherman DG, Albers GW, Bladin C, Fieschi C, Gabbai AA, Kase CS, et al. The efficacy and safety of enoxaparin versus unfractionated heparin for the prevention of venous thromboembolism after acute ischaemic stroke (PREVAIL Study): an open-label randomised comparison. Lancet. 2007;369(9570):1347–55.PubMedCrossRefGoogle Scholar
  23. 23.
    Dennis M, Sandercock P, Reid J, Graham C, Murray G, Venables G, et al. The effect of graduated compression stockings on long-term outcomes after stroke: the CLOTS trials 1 and 2. Stroke. 2013;44(4):1075–9.PubMedCrossRefGoogle Scholar
  24. 24.
    Dennis M, Sandercock P, Reid J, Graham C, Forbes J, Murray G. Effectiveness of intermittent pneumatic compression in reduction of risk of deep vein thrombosis in patients who have had a stroke (CLOTS 3): a multicentre randomised controlled trial. Lancet. 2013;382(9891):516–24.PubMedCrossRefGoogle Scholar
  25. 25.
    Sandercock PA, van den Belt AG, Lindley RI, Slattery J. Antithrombotic therapy in acute ischaemic stroke: an overview of the completed randomised trials. J Neurol Neurosurg Psychiatry. 1993;56(1):17–25.PubMedCentralPubMedCrossRefGoogle Scholar
  26. 26.
    Gould MK, Dembitzer AD, Doyle RL, Hastie TJ, Garber AM. Low-molecular-weight heparins compared with unfractionated heparin for treatment of acute deep venous thrombosis. A meta-analysis of randomized, controlled trials. Ann Intern Med. 1999;130(10):800–9.PubMedCrossRefGoogle Scholar
  27. 27.
    Geerts WH, Pineo GF, Heit JA, Bergqvist D, Lassen MR, Colwell CW, et al. Prevention of venous thromboembolism: the seventh ACCP conference on antithrombotic and thrombolytic therapy. Chest. 2004;126(3 Suppl):338S–400S.Google Scholar
  28. 28.
    Kamphuisen PW, Agnelli G, Sebastianelli M. Prevention of venous thromboembolism after acute ischemic stroke. J Thromb Haemost. 2005;3(6):1187–94.PubMedCrossRefGoogle Scholar
  29. 29.
    Mazzone C, Chiodo GF, Sandercock P, Miccio M, Salvi R. Physical methods for preventing deep vein thrombosis in stroke. Cochrane Database Syst Rev. 2004(4):CD001922.Google Scholar
  30. 30.
    Kamran SI, Downey D, Ruff RL. Pneumatic sequential compression reduces the risk of deep vein thrombosis in stroke patients. Neurology. 1998;50(6):1683–8.PubMedCrossRefGoogle Scholar
  31. 31.
    Nicolaides AN, Fareed J, Kakkar AK, Breddin HK, Goldhaber SZ, Hull R, et al. Prevention and treatment of venous thromboembolism International Consensus Statement (Guidelines according to scientific evidence). Int Angiol. 2006;25(2):101–61.Google Scholar
  32. 32.
    Epstein NE. A review of the risks and benefits of differing prophylaxis regimens for the treatment of deep venous thrombosis and pulmonary embolism in neurosurgery. Surg Neurol. 2005;64(4):295–301.PubMedCrossRefGoogle Scholar
  33. 33.
    Agnelli G. Prevention of venous thromboembolism after neurosurgery. Thromb Haemost. 1999;82(2):925–30.PubMedGoogle Scholar
  34. 34.
    Frim DM, Barker FG, Poletti CE, Hamilton AJ. Postoperative low-dose heparin decreases thromboembolic complications in neurosurgical patients. Neurosurgery. 1992;30(6):830–2.PubMedCrossRefGoogle Scholar
  35. 35.
    Goldstein JN, Fazen LE, Wendell L, Chang Y, Rost NS, Snider R, et al. Risk of thromboembolism following acute intracerebral hemorrhage. Neurocrit Care. 2009;10(1):28–34.PubMedCentralPubMedCrossRefGoogle Scholar
  36. 36.
    Gregory PC, Kuhlemeier KV. Prevalence of venous thromboembolism in acute hemorrhagic and thromboembolic stroke. Am J Phys Med Rehabil. 2003;82(5):364–9.PubMedGoogle Scholar
  37. 37.
    Kim KS, Brophy GM. Symptomatic venous thromboembolism: incidence and risk factors in patients with spontaneous or traumatic intracranial hemorrhage. Neurocrit Care. 2009;11(1):28–33.PubMedCrossRefGoogle Scholar
  38. 38.
    Skaf E, Stein PD, Beemath A, Sanchez J, Bustamante MA, Olson RE. Venous thromboembolism in patients with ischemic and hemorrhagic stroke. Am J Cardiol. 2005;96(12):1731–3.PubMedCrossRefGoogle Scholar
  39. 39.
    Diringer MN, Skolnick BE, Mayer SA, Steiner T, Davis SM, Brun NC, et al. Thromboembolic events with recombinant activated factor VII in spontaneous intracerebral hemorrhage: results from the factor seven for acute hemorrhagic stroke (FAST) trial. Stroke. 2010;41(1):48–53.PubMedCrossRefGoogle Scholar
  40. 40.
    Kawase K, Okazaki S, Toyoda K, Toratani N, Yoshimura S, Kawano H, et al. Sex difference in the prevalence of deep-vein thrombosis in Japanese patients with acute intracerebral hemorrhage. Cerebrovasc Dis. 2009;27(4):313–9.PubMedCrossRefGoogle Scholar
  41. 41.
    Ogata T, Yasaka M, Wakugawa Y, Inoue T, Ibayashi S, Okada Y. Deep venous thrombosis after acute intracerebral hemorrhage. J Neurol Sci. 2008;272(1–2):83–6.PubMedCrossRefGoogle Scholar
  42. 42.
    Lyden PD, Shuaib A, Lees KR, Davalos A, Davis SM, Diener HC, et al. Safety and tolerability of NXY-059 for acute intracerebral hemorrhage: the CHANT Trial. Stroke. 2007;38(8):2262–9.PubMedCrossRefGoogle Scholar
  43. 43.
    Maramattom BV, Weigand S, Reinalda M, Wijdicks EF, Manno EM. Pulmonary complications after intracerebral hemorrhage. Neurocrit Care. 2006;5(2):115–9.PubMedCrossRefGoogle Scholar
  44. 44.
    Lacut K, Bressollette L, Le Gal G, Etienne E, De Tinteniac A, Renault A, et al. Prevention of venous thrombosis in patients with acute intracerebral hemorrhage. Neurology. 2005;65(6):865–9.PubMedCrossRefGoogle Scholar
  45. 45.
    Dennis M, Sandercock PA, Reid J, Graham C, Murray G, Venables G, et al. Effectiveness of thigh-length graduated compression stockings to reduce the risk of deep vein thrombosis after stroke (CLOTS trial 1): a multicentre, randomised controlled trial. Lancet. 2009;373(9679):1958–65.PubMedCrossRefGoogle Scholar
  46. 46.
    Boeer A, Voth E, Henze T, Prange HW. Early heparin therapy in patients with spontaneous intracerebral haemorrhage. J Neurol Neurosurg Psychiatry. 1991;54(5):466–7.PubMedCentralPubMedCrossRefGoogle Scholar
  47. 47.
    Orken DN, Kenangil G, Ozkurt H, Guner C, Gundogdu L, Basak M, et al. Prevention of deep venous thrombosis and pulmonary embolism in patients with acute intracerebral hemorrhage. Neurologist. 2009;15(6):329–31.PubMedCrossRefGoogle Scholar
  48. 48.
    O’Carroll CB, Capampangan DJ, Aguilar MI, Bravo TP, Hoffman-Snyder CR, Wingerchuk DM, et al. What is the effect of low-molecular weight heparin for venous thromboembolism prophylaxis compared with mechanical methods, on the occurrence of hemorrhagic and venous thromboembolic complications in patients with intracerebral hemorrhage? A critically appraised topic. Neurologist. 2011;17(4):232–5.PubMedCrossRefGoogle Scholar
  49. 49.
    Paciaroni M, Agnelli G, Venti M, Alberti A, Acciarresi M, Caso V. Efficacy and safety of anticoagulants in the prevention of venous thromboembolism in patients with acute cerebral hemorrhage: a meta-analysis of controlled studies. J. Thromb Haemost. 2011;9(5):893–8.PubMedCrossRefGoogle Scholar
  50. 50.
    Tetri S, Hakala J, Juvela S, Saloheimo P, Pyhtinen J, Rusanen H, et al. Safety of low-dose subcutaneous enoxaparin for the prevention of venous thromboembolism after primary intracerebral haemorrhage. Thromb Res. 2008;123(2):206–12.PubMedCrossRefGoogle Scholar
  51. 51.
    Wasay M, Khan S, Zaki KS, Khealani BA, Kamal A, Azam I, et al. A non-randomized study of safety and efficacy of heparin for DVT prophylaxis in intracerebral haemorrhage. J Pak Med Assoc. 2008;58(7):362–4.PubMedGoogle Scholar
  52. 52.
    Lansberg MG, O’Donnell MJ, Khatri P, Lang ES, Nguyen-Huynh MN, Schwartz NE, et al. Antithrombotic and thrombolytic therapy for ischemic stroke: antithrombotic therapy and prevention of thrombosis, 9th ed: American College of Chest Physicians evidence-based clinical practice guidelines. Chest. 2012;141(2 Suppl):e601S–36S.PubMedCentralPubMedCrossRefGoogle Scholar
  53. 53.
    Dickmann U, Voth E, Schicha H, Henze T, Prange H, Emrich D. Heparin therapy, deep-vein thrombosis and pulmonary embolism after intracerebral hemorrhage. Klinische Wochenschr. 1988;66(23):1182–3.CrossRefGoogle Scholar
  54. 54.
    Kshettry VR, Rosenbaum BP, Seicean A, Kelly ML, Schiltz NK, Weil RJ. Incidence and risk factors associated with in-hospital venous thromboembolism after aneurysmal subarachnoid hemorrhage. J Clin Neurosci. 2014;21(2):282–6.PubMedCrossRefGoogle Scholar
  55. 55.
    Ray WZ, Strom RG, Blackburn SL, Ashley WW, Sicard GA, Rich KM. Incidence of deep venous thrombosis after subarachnoid hemorrhage. J Neurosurg. 2009;110(5):1010–4.PubMedCrossRefGoogle Scholar
  56. 56.
    Mack WJ, Ducruet AF, Hickman ZL, Kalyvas JT, Cleveland JR, Mocco J, et al. Doppler ultrasonography screening of poor-grade subarachnoid hemorrhage patients increases the diagnosis of deep venous thrombosis. Neurol Res. 2008;30(9):889–92.PubMedCrossRefGoogle Scholar
  57. 57.
    Vespa P. Deep venous thrombosis prophylaxis. Neurocrit Care. 2011;15(2):295–7.PubMedCrossRefGoogle Scholar
  58. 58.
    Olkowski BF, Devine MA, Slotnick LE, Veznedaroglu E, Liebman KM, Arcaro ML, et al. Safety and feasibility of an early mobilization program for patients with aneurysmal subarachnoid hemorrhage. Phys Ther. 2013;93(2):208–15.PubMedCrossRefGoogle Scholar
  59. 59.
    Collen JF, Jackson JL, Shorr AF, Moores LK. Prevention of venous thromboembolism in neurosurgery: a metaanalysis. Chest. 2008;134(2):237–49.PubMedCrossRefGoogle Scholar
  60. 60.
    Qaseem A, Chou R, Humphrey LL, Starkey M, Shekelle P. Clinical Guidelines Committee of the American College of P. Venous thromboembolism prophylaxis in hospitalized patients: a clinical practice guideline from the American College of Physicians. Ann Intern Med. 2011;155(9):625–32.PubMedCrossRefGoogle Scholar
  61. 61.
    Abdullah JM, Zainuddin N, Sulong S, Jaafar H, Isa MN. Molecular genetic analysis of phosphatase and tensin homolog and p16 tumor suppressor genes in patients with malignant glioma. Neurosurg Focus. 2003;14(4):e6.PubMedCrossRefGoogle Scholar
  62. 62.
    Diringer MN, Bleck TP, Claude Hemphill J, 3rd, Menon D, Shutter L, Vespa P, et al. Critical care management of patients following aneurysmal subarachnoid hemorrhage: recommendations from the Neurocritical Care Society’s Multidisciplinary Consensus Conference. Neurocrit Care. 2011;15(2):211–40.Google Scholar
  63. 63.
    Gould MK, Garcia DA, Wren SM, Karanicolas PJ, Arcelus JI, Heit JA, et al. Prevention of VTE in nonorthopedic surgical patients: Antithrombotic therapy and prevention of thrombosis, 9th ed: American College of Chest Physicians evidence-based clinical practice guidelines. Chest. 2012;141(2 Suppl):e227S–77S.PubMedCentralPubMedCrossRefGoogle Scholar
  64. 64.
    Geerts WH, Bergqvist D, Pineo GF, Heit JA, Samama CM, Lassen MR, et al. Prevention of venous thromboembolism: American College of Chest Physicians evidence-based clinical practice guidelines (8th Edition). Chest. 2008;133(6 Suppl):381S–453S.PubMedCrossRefGoogle Scholar
  65. 65.
    Gearhart MM, Luchette FA, Proctor MC, Lutomski DM, Witsken C, James L, et al. The risk assessment profile score identifies trauma patients at risk for deep vein thrombosis. Surgery. 2000;128(4):631–40.PubMedCrossRefGoogle Scholar
  66. 66.
    Knudson MM, Ikossi DG, Khaw L, Morabito D, Speetzen LS. Thromboembolism after trauma: an analysis of 1602 episodes from the American College of Surgeons National Trauma Data Bank. Ann Surg. 2004;240(3):490–6.Google Scholar
  67. 67.
    Sharma OP, Oswanski MF, Joseph RJ, Tonui P, Westrick L, Raj SS, et al. Venous thromboembolism in trauma patients. Am Surg. 2007;73(11):1173–80.PubMedGoogle Scholar
  68. 68.
    Imberti D, Ageno W. A survey of thromboprophylaxis management in patients with major trauma. Pathophysiol Haemost Thromb. 2005;34(6):249–54.PubMedCrossRefGoogle Scholar
  69. 69.
    Nathens AB, McMurray MK, Cuschieri J, Durr EA, Moore EE, Bankey PE, et al. The practice of venous thromboembolism prophylaxis in the major trauma patient. J Trauma. 2007;62(3):557–62.Google Scholar
  70. 70.
    Reiff DA, Haricharan RN, Bullington NM, Griffin RL, McGwin G Jr, Rue LW 3rd. Traumatic brain injury is associated with the development of deep vein thrombosis independent of pharmacological prophylaxis. J Trauma. 2009;66(5):1436–40.PubMedCrossRefGoogle Scholar
  71. 71.
    Rogers FB, Cipolle MD, Velmahos G, Rozycki G, Luchette FA. Practice management guidelines for the prevention of venous thromboembolism in trauma patients: the EAST practice management guidelines work group. J Trauma. 2002;53(1):142–64.PubMedCrossRefGoogle Scholar
  72. 72.
    Bratton SL, Chestnut RM, Ghajar J, McConnell Hammond FF, Harris OA, Hartl R, et al. Guidelines for the management of severe traumatic brain injury. II. Hyperosmolar therapy. J Neurotrauma. 2007;24(Suppl 1):S14–20.PubMedGoogle Scholar
  73. 73.
    Simanek R, Vormittag R, Hassler M, Roessler K, Schwarz M, Zielinski C, et al. Venous thromboembolism and survival in patients with high-grade glioma. Neuro-oncology. 2007;9(2):89–95.PubMedCentralPubMedCrossRefGoogle Scholar
  74. 74.
    Robins HI, O’Neill A, Gilbert M, Olsen M, Sapiente R, Berkey B, et al. Effect of dalteparin and radiation on survival and thromboembolic events in glioblastoma multiforme: a phase II ECOG trial. Cancer Chemother Pharmacol. 2008;62(2):227–33.PubMedCentralPubMedCrossRefGoogle Scholar
  75. 75.
    Perry SL, Bohlin C, Reardon DA, Desjardins A, Friedman AH, Friedman HS, et al. Tinzaparin prophylaxis against venous thromboembolic complications in brain tumor patients. J Neurooncol. 2009;95(1):129–34.PubMedCentralPubMedCrossRefGoogle Scholar
  76. 76.
    Perry JR, Julian JA, Laperriere NJ, Geerts W, Agnelli G, Rogers LR, et al. PRODIGE: a randomized placebo-controlled trial of dalteparin low-molecular-weight heparin thromboprophylaxis in patients with newly diagnosed malignant glioma. J Thromb Haemost. 2010;8(9):1959–65.PubMedCrossRefGoogle Scholar
  77. 77.
    Cage TA, Lamborn KR, Ware ML, Frankfurt A, Chakalian L, Berger MS, et al. Adjuvant enoxaparin therapy may decrease the incidence of postoperative thrombotic events though does not increase the incidence of postoperative intracranial hemorrhage in patients with meningiomas. J Neurooncol. 2009;93(1):151–6.PubMedCrossRefGoogle Scholar
  78. 78.
    Miranda AR, Hassouna HI. Mechanisms of thrombosis in spinal cord injury. Hematol Oncol Clin North Am. 2000;14(2):401–16.PubMedCrossRefGoogle Scholar
  79. 79.
    Aito S, Pieri A, D’Andrea M, Marcelli F, Cominelli E. Primary prevention of deep venous thrombosis and pulmonary embolism in acute spinal cord injured patients. Spinal Cord. 2002;40(6):300–3.PubMedCrossRefGoogle Scholar
  80. 80.
    Green D, Lee MY, Lim AC, Chmiel JS, Vetter M, Pang T, et al. Prevention of thromboembolism after spinal cord injury using low-molecular-weight heparin. Ann Intern Med. 1990;113(8):571–4.PubMedCrossRefGoogle Scholar
  81. 81.
    Merli GJ, Crabbe S, Doyle L, Ditunno JF, Herbision GJ. Mechanical plus pharmacological prophylaxis for deep vein thrombosis in acute spinal cord injury. Paraplegia. 1992;30(8):558–62.PubMedCrossRefGoogle Scholar
  82. 82.
    Wilson JT, Rogers FB, Wald SL, Shackford SR, Ricci MA. Prophylactic vena cava filter insertion in patients with traumatic spinal cord injury: preliminary results. Neurosurgery. 1994;35(2):234–9.Google Scholar
  83. 83.
    Khansarinia S, Dennis JW, Veldenz HC, Butcher JL, Hartland L. Prophylactic Greenfield filter placement in selected high-risk trauma patients. J Vasc Surg. 1995;22(3):231–5.PubMedCrossRefGoogle Scholar
  84. 84.
    Rogers FB, Shackford SR, Ricci MA, Wilson JT, Parsons S. Routine prophylactic vena cava filter insertion in severely injured trauma patients decreases the incidence of pulmonary embolism. J Am Coll Surg. 1995;180(6):641–7.PubMedGoogle Scholar
  85. 85.
    Harris S, Chen D, Green D. Enoxaparin for thromboembolism prophylaxis in spinal injury: preliminary report on experience with 105 patients. Am J Phys Med Rehabil. 1996;75(5):326–7.PubMedCrossRefGoogle Scholar
  86. 86.
    Geerts WH, Jay RM, Code KI, Chen E, Szalai JP, Saibil EA, et al. A comparison of low-dose heparin with low-molecular-weight heparin as prophylaxis against venous thromboembolism after major trauma. N Engl J Med. 1996;335(10):701–7.PubMedCrossRefGoogle Scholar
  87. 87.
    Consortium for Spinal Cord Medicine. Prevention of thromboembolism in spinal cord injury. 2nd ed. Washington, DC: Paralyzed Veterans of America; 1999.Google Scholar
  88. 88.
    Worley S, Short C, Pike J, Anderson D, Douglas JA, Thompson K. Dalteparin vs low-dose unfractionated heparin for prophylaxis against clinically evident venous thromboembolism in acute traumatic spinal cord injury: a retrospective cohort study. Journal Spinal Cord Med. 2008;31(4):379–87.Google Scholar
  89. 89.
    Wade WE, Chisholm MA. Venous thrombosis after acute spinal cord injury: cost analysis of prophylaxis guidelines. Am J Phys Med Rehabil. 2000;79(6):504–8.PubMedCrossRefGoogle Scholar
  90. 90.
    Kahn SR, Lim W, Dunn AS, Cushman M, Dentali F, Akl EA, et al. Prevention of vte in nonsurgical patients: Antithrombotic therapy and prevention of thrombosis, 9th ed: american college of chest physicians evidence-based clinical practice guidelines. Chest. 2012;141(2_suppl):e195S-e226S.Google Scholar
  91. 91.
    Gaber TA, Kirker SG, Jenner JR. Current practice of prophylactic anticoagulation in Guillain–Barre syndrome. Clin Rehabil. 2002;16(2):190–3.PubMedCrossRefGoogle Scholar
  92. 92.
    Henderson RD, Lawn ND, Fletcher DD, McClelland RL, Wijdicks EF. The morbidity of Guillain–Barre syndrome admitted to the intensive care unit. Neurology. 2003;60(1):17–21.PubMedCrossRefGoogle Scholar
  93. 93.
    Hewer RL, Hilton PJ, Smith AC, Spalding JM. Acute polyneuritis requiring artificial respiration. Q J Med. 1968;37(147):479–91.PubMedGoogle Scholar
  94. 94.
    Ng KK, Howard RS, Fish DR, Hirsch NP, Wiles CM, Murray NM, et al. Management and outcome of severe Guillain–Barre syndrome. QJM Mon J Assoc Physicians. 1995;88(4):243–50.Google Scholar
  95. 95.
    Moore P, James O. Guillain–Barre syndrome: incidence, management and outcome of major complications. Crit Care Med. 1981;9(7):549–55.PubMedCrossRefGoogle Scholar
  96. 96.
    Ropper AH, Kehne SM. Guillain–Barre syndrome: management of respiratory failure. Neurology. 1985;35(11):1662–5.PubMedCrossRefGoogle Scholar
  97. 97.
    Alikhan R, Cohen AT. Heparin for the prevention of venous thromboembolism in general medical patients (excluding stroke and myocardial infarction). Cochrane Database Syst Rev. 2009(3):CD003747.Google Scholar
  98. 98.
    King CS, Holley AB, Jackson JL, Shorr AF, Moores LK. Twice vs three times daily heparin dosing for thromboembolism prophylaxis in the general medical population: a metaanalysis. Chest. 2007;131(2):507–16.PubMedCrossRefGoogle Scholar
  99. 99.
    Phung OJ, Kahn SR, Cook DJ, Murad MH. Dosing frequency of unfractionated heparin thromboprophylaxis: a meta-analysis. Chest. 2011;140(2):374–81.PubMedCrossRefGoogle Scholar
  100. 100.
    Wein L, Wein S, Haas SJ, Shaw J, Krum H. Pharmacological venous thromboembolism prophylaxis in hospitalized medical patients: a meta-analysis of randomized controlled trials. Arch Intern Med. 2007;167(14):1476–86.PubMedCrossRefGoogle Scholar
  101. 101.
    Kakkos SK, Caprini JA, Geroulakos G, Nicolaides AN, Stansby GP, Reddy DJ. Combined intermittent pneumatic leg compression and pharmacological prophylaxis for prevention of venous thromboembolism in high-risk patients. Cochrane Database Syst Rev. 2008(4):CD005258.Google Scholar
  102. 102.
    Sachdeva A, Dalton M, Amaragiri SV, Lees T. Elastic compression stockings for prevention of deep vein thrombosis. Cochrane Database Syst Rev. 2010(7):CD001484.Google Scholar
  103. 103.
    Cook D, Meade M, Guyatt G, Walter S, Heels-Ansdell D, Warkentin TE, et al. Dalteparin versus unfractionated heparin in critically ill patients. N Engl J Med. 2011;364(14):1305–14.PubMedCrossRefGoogle Scholar
  104. 104.
    Dearborn JT, Hu SS, Tribus CB, Bradford DS. Thromboembolic complications after major thoracolumbar spine surgery. Spine. 1999;24(14):1471–6.PubMedCrossRefGoogle Scholar
  105. 105.
    Glotzbecker MP, Bono CM, Wood KB, Harris MB. Thromboembolic disease in spinal surgery: a systematic review. Spine. 2009;34(3):291–303.PubMedCrossRefGoogle Scholar
  106. 106.
    Geerts WH, Heit JA, Clagett GP, Pineo GF, Colwell CW, Anderson FA Jr, et al. Prevention of venous thromboembolism. Chest. 2001;119(1 Suppl):132S–75S.PubMedCrossRefGoogle Scholar
  107. 107.
    Agnelli G. Prevention of venous thromboembolism in surgical patients. Circulation. 2004;110(24 Suppl 1):IV4–12.Google Scholar
  108. 108.
    Smith JS, Fu KMG, Polly DW, Sansur CA, Berven SH, Broadstone PA, et al. Complication rates of three common spine procedures and rates of thromboembolism following spine surgery based on 108,419 procedures: a report from the scoliosis research society morbidity and mortality committee. Spine. 2010;35(24):2140–9.PubMedCrossRefGoogle Scholar
  109. 109.
    Quevedo JF, Buckner JC, Schmidt JL, Dinapoli RP, O’Fallon JR. Thromboembolism in patients with high-grade glioma. Mayo Clin Proc. 1994;69(4):329–32.PubMedCrossRefGoogle Scholar
  110. 110.
    Semrad TJ, O’Donnell R, Wun T, Chew H, Harvey D, Zhou H, et al. Epidemiology of venous thromboembolism in 9489 patients with malignant glioma. J Neurosurg. 2007;106(4):601–8.PubMedCrossRefGoogle Scholar
  111. 111.
    Iorio A, Agnelli G. Low-molecular-weight and unfractionated heparin for prevention of venous thromboembolism in neurosurgery: a meta-analysis. Arch Intern Med. 2000;160(15):2327–32.PubMedCrossRefGoogle Scholar
  112. 112.
    Agnelli G, Piovella F, Buoncristiani P, Severi P, Pini M, D’Angelo A, et al. Enoxaparin plus compression stockings compared with compression stockings alone in the prevention of venous thromboembolism after elective neurosurgery. N Engl J Med. 1998;339(2):80–5.PubMedCrossRefGoogle Scholar
  113. 113.
    Nurmohamed MT, van Riel AM, Henkens CM, Koopman MM, Que GT, d’Azemar P, et al. Low molecular weight heparin and compression stockings in the prevention of venous thromboembolism in neurosurgery. Thromb Haemost. 1996;75(2):233–8.PubMedGoogle Scholar
  114. 114.
    Paoletti C, Maubec E, Raggueneau JL, George B, Robine D, Matheron R, et al. [Clinical tolerance of CY 216 (Fraxiparin) in the prevention of thromboembolic accidents after neurosurgery]. Agressologie: revue internationale de physio-biologie et de pharmacologie appliquees aux effets de l’agression. 1989;30(6):363–6.Google Scholar
  115. 115.
    Voth D, Schwarz M, Hahn K, Dei-Anang K, al Butmeh S, Wolf H. Prevention of deep vein thrombosis in neurosurgical patients: a prospective double-blind comparison of two prophylactic regimen. Neurosurgical review. 1992;15(4):289–94.Google Scholar
  116. 116.
    Barnett HG, Clifford JR, Llewellyn RC. Safety of mini-dose heparin administration for neurosurgical patients. J Neurosurg. 1977;47(1):27–30.PubMedCrossRefGoogle Scholar
  117. 117.
    Bostrom S, Holmgren E, Jonsson O, Lindberg S, Lindstrom B, Winso I, et al. Post-operative thromboembolism in neurosurgery. A study on the prophylactic effect of calf muscle stimulation plus dextran compared to low-dose heparin. Acta Neurochir (Wien). 1986;80(3–4):83–9.CrossRefGoogle Scholar
  118. 118.
    Cerrato D, Ariano C, Fiacchino F. Deep vein thrombosis and low-dose heparin prophylaxis in neurosurgical patients. J Neurosurg. 1978;49(3):378–81.PubMedCrossRefGoogle Scholar
  119. 119.
    Bynke O, Hillman J, Lassvik C. Does peroperative external pneumatic leg muscle compression prevent post-operative venous thrombosis in neurosurgery? Acta Neurochir (Wien). 1987;88(1–2):46–8.CrossRefGoogle Scholar
  120. 120.
    Skillman JJ, Collins RE, Coe NP, Goldstein BS, Shapiro RM, Zervas NT, et al. Prevention of deep vein thrombosis in neurosurgical patients: a controlled, randomized trial of external pneumatic compression boots. Surgery. 1978;83(3):354–8.PubMedGoogle Scholar
  121. 121.
    Kshettry VR, Rosenbaum BP, Seicean A, Kelly ML, Schiltz NK, Weil RJ. Incidence and risk factors associated with in-hospital venous thromboembolism after aneurysmal subarachnoid hemorrhage. J Clin Neurosci. 2014;21(2):282–6. doi: 10.1016/j.jocn.2013.07.003.PubMedCrossRefGoogle Scholar
  122. 122.
    Epstein NE. Efficacy of pneumatic compression stocking prophylaxis in the prevention of deep venous thrombosis and pulmonary embolism following 139 lumbar laminectomies with instrumented fusions. J Spinal Disord Tech. 2006;19(1):28–31.PubMedCrossRefGoogle Scholar
  123. 123.
    Nelson LD Jr, Montgomery SP, Dameron TB Jr, Nelson RB. Deep vein thrombosis in lumbar spinal fusion: a prospective study of antiembolic and pneumatic compression stockings. J South Orthop Assoc. 1996;5(3):181–4.PubMedGoogle Scholar
  124. 124.
    Turpie AG, Hirsh J, Gent M, Julian D, Johnson J. Prevention of deep vein thrombosis in potential neurosurgical patients. A randomized trial comparing graduated compression stockings alone or graduated compression stockings plus intermittent pneumatic compression with control. Arch Intern Med. 1989;149(3):679–81.PubMedCrossRefGoogle Scholar
  125. 125.
    Wood KB, Kos PB, Abnet JK, Ista C. Prevention of deep-vein thrombosis after major spinal surgery: a comparison study of external devices. J Spinal Disord. 1997;10(3):209–14.PubMedCrossRefGoogle Scholar
  126. 126.
    Ferree BA, Wright AM. Deep venous thrombosis following posterior lumbar spinal surgery. Spine. 1993;18(8):1079–82.PubMedCrossRefGoogle Scholar
  127. 127.
    Ferree BA. Deep venous thrombosis following lumbar laminotomy and laminectomy. Orthopedics. 1994;17(1):35–8.PubMedGoogle Scholar
  128. 128.
    Ferree BA, Stern PJ, Jolson RS, Roberts JM, Kahn A III. Deep venous thrombosis after spinal surgery. Spine. 1993;18(3):315–9.PubMedCrossRefGoogle Scholar
  129. 129.
    Wen DY, Hall WA. Complications of subcutaneous low-dose heparin therapy in neurosurgical patients. Surg Neurol. 1998;50(6):521–5.PubMedCrossRefGoogle Scholar
  130. 130.
    Dickinson LD, Miller LD, Patel CP, Gupta SK. Enoxaparin increases the incidence of postoperative intracranial hemorrhage when initiated preoperatively for deep venous thrombosis prophylaxis in patients with brain tumors. Neurosurgery. 1998;43(5):1074–81.PubMedCrossRefGoogle Scholar
  131. 131.
    Constantini S, Kanner A, Friedman A, Shoshan Y, Israel Z, Ashkenazi E, et al. Safety of perioperative minidose heparin in patients undergoing brain tumor surgery: a prospective, randomized, double-blind study. J Neurosurg. 2001;94(6):918–21.PubMedCrossRefGoogle Scholar
  132. 132.
    Macdonald RL, Amidei C, Baron J, Weir B, Brown F, Erickson RK, et al. Randomized, pilot study of intermittent pneumatic compression devices plus dalteparin versus intermittent pneumatic compression devices plus heparin for prevention of venous thromboembolism in patients undergoing craniotomy. Surg Neurol. 2003;59(5):363–72.Google Scholar
  133. 133.
    Macdonald RL, Amidei C, Lin G, Munshi I, Baron J, Weir BK, et al. Safety of perioperative subcutaneous heparin for prophylaxis of venous thromboembolism in patients undergoing craniotomy. Neurosurgery. 1999;45(2):245–51.Google Scholar
  134. 134.
    Minshall CT, Eriksson EA, Leon SM, Doben AR, McKinzie BP, Fakhry SM. Safety and efficacy of heparin or enoxaparin prophylaxis in blunt trauma patients with a head abbreviated injury severity score > 2. J Trauma. 2011;71(2):396–9.Google Scholar
  135. 135.
    Nurmohamed MT, ten Cate H, ten Cate JW. Low molecular weight heparin(oid)s. Clinical investigations and practical recommendations. Drugs. 1997;53(5):736–51.PubMedCrossRefGoogle Scholar
  136. 136.
    Rokito SE, Schwartz MC, Neuwirth MG. Deep vein thrombosis after major reconstructive spinal surgery. Spine. 1996;21(7):853–8.Google Scholar
  137. 137.
    Rosner MK, Kuklo TR, Tawk R, Moquin R, Ondra SL. Prophylactic placement of an inferior vena cava filter in high-risk patients undergoing spinal reconstruction. Neurosurg Focus. 2004;17(4):E6.PubMedCrossRefGoogle Scholar
  138. 138.
    Ozturk C, Ganiyusufoglu K, Alanay A, Aydogan M, Onat L, Hamzaoglu A. Efficacy of prophylactic placement of inferior vena cava filter in patients undergoing spinal surgery. Spine. 2010;35(20):1893–6.PubMedCrossRefGoogle Scholar
  139. 139.
    Gorman PH, Qadri SF, Rao-Patel A. Prophylactic inferior vena cava (IVC) filter placement may increase the relative risk of deep venous thrombosis after acute spinal cord injury. J Trauma. 2009;66(3):707–12.PubMedCrossRefGoogle Scholar
  140. 140.
    Britt LD, Zolfaghari D, Kennedy E, Pagel KJ, Minghini A. Incidence and prophylaxis of deep vein thrombosis in a high risk trauma population. Am J Surg. 1996;172(1):13–4.PubMedCrossRefGoogle Scholar
  141. 141.
    Goldhaber SZ, Dunn K, Gerhard-Herman M, Park JK, Black PM. Low rate of venous thromboembolism after craniotomy for brain tumor using multimodality prophylaxis. Chest. 2002;122(6):1933–7.PubMedCrossRefGoogle Scholar
  142. 142.
    Hoh BL, Nogueira RG, Ledezma CJ, Pryor JC, Ogilvy CS. Safety of heparinization for cerebral aneurysm coiling soon after external ventriculostomy drain placement. Neurosurgery. 2005;57(5):845–9.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  • Paul Nyquist
    • 1
    Email author
  • Cynthia Bautista
    • 2
  • Draga Jichici
    • 3
  • Joseph Burns
    • 4
  • Sanjeev Chhangani
    • 5
  • Michele DeFilippis
    • 6
  • Fernando D. Goldenberg
    • 7
  • Keri Kim
    • 8
  • Xi Liu-DeRyke
    • 9
  • William Mack
    • 10
  • Kim Meyer
    • 11
  1. 1.Departments of Neurology, Anesthesia/Critical Care Medicine, Neurosurgery, and General Internal MedicineJohn Hopkins School of MedicineBaltimoreUSA
  2. 2.Department of Nursing, Neuroscience CNSYale-New Haven HospitalNew HavenUSA
  3. 3.Department of Neurology and Critical CareMcMaster UniversityHamiltonCanada
  4. 4.Department of NeurologyLahey Hospital and Medical CenterBurlingtonUSA
  5. 5.Department of AnesthesiaCritical Care and Pain MedicineBostonUSA
  6. 6.Department of NursingMorristown Medical CenterMorristownUSA
  7. 7.Department of NeurologyThe University of Chicago MedicineChicagoUSA
  8. 8.Department of NeurosurgeryUniversity of Illinois Hospital & Health Sciences SystemChicagoUSA
  9. 9.Division of Surgical Critical CareOrlando Regional Medical CenterOrlandoUSA
  10. 10.Department of NeurosurgeryLos Angeles County University Southern California Medical CenterLos AngelesUSA
  11. 11.Department of NeurosurgeryUniversity of Louisville PhysiciansLouisvilleUSA

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