Journal of Neuro-Oncology

, Volume 120, Issue 3, pp 567–573 | Cite as

Risk factors for venous thromboembolism in patients undergoing craniotomy for neoplastic disease

Clinical Study

Abstract

Patients undergoing neurosurgical procedures for neoplasia have historically been considered at higher risk for developing venous thromboembolism (VTE). We sought to identify risk factors associated with VTE in patients undergoing craniotomy for tumor resection. We reviewed a national surgical quality database (American College of Surgeons National Surgical Quality Improvement Project, ACS-NSQIP, http://site.acsnsqip.org/). Patients undergoing non-emergent craniotomy for neoplastic indications were identified based on current procedural terminology codes. Clinical factors were identified that were associated with VTE events. 3,098 patients who underwent non-emergent craniotomy were identified. 1,741 patients underwent procedures for neoplastic disease (56.2 %). The rate of DVT in these patients was 3.2 % compared to 1.4 % in other neurosurgical patients (OR 2.30, CI 2.29–2.30). The rate of pulmonary embolism was 1.8 % compared to 0.5 % (OR 3.61, CI 3.60–3.62). Univariate analysis identified several factors correlated with VTE. Pre-operative characteristics associated with VTE were the presence of impaired sensorium, dependent functional status, and age > 60 years. Total operative time > 4 h was associated with VTE. Post-operative events associated with VTE included pneumonia, unplanned intubation, fail to wean from ventilator, UTI, stroke, sepsis and septic shock. Age > 60, OR time > 4 h, UTI, and septic shock were significantly associated with VTE in multivariate analysis. Patients undergoing craniotomy for neoplasm are at increased risk of VTE. This risk appears to be modified by pre-operative medical comorbidities, longer operative time, and post-operative complications.

Keywords

ACS-NSQIP Venous thromboembolism Risk factors Craniotomy Brain tumor 

References

  1. 1.
    Agnelli G (2004) Prevention of venous thromboembolism in surgical patients. Circulation 110(24 Suppl 1):IV4–12. doi:10.1161/01.CIR.0000150639.98514.6c PubMedGoogle Scholar
  2. 2.
    Hamilton MG, Yee WH, Hull RD, Ghali WA (2011) Venous thromboembolism prophylaxis in patients undergoing cranial neurosurgery: a systematic review and meta-analysis. Neurosurgery 68(3):571–581. doi:10.1227/NEU.0b013e3182093145 PubMedCrossRefGoogle Scholar
  3. 3.
    Collen JF, Jackson JL, Shorr AF, Moores LK (2008) Prevention of venous thromboembolism in neurosurgery: a metaanalysis. Chest 134(2):237–249. doi:10.1378/chest.08-0023 PubMedCrossRefGoogle Scholar
  4. 4.
    National Surgical Quality Improvement Program (2012) User guide for the 2011 participant use data file. American College of Surgeons. http://site.acsnsqip.org/wp-content/uploads/2012/03/2011-User-Guide_Final.pdf. Accessed 21 Aug 2014
  5. 5.
    Owens WD, Felts JA, Spitznagel EL Jr (1978) ASA physical status classifications: a study of consistency of ratings. Anesthesiology 49(4):239–243PubMedCrossRefGoogle Scholar
  6. 6.
    Mallampati SR, Gatt SP, Gugino LD, Desai SP, Waraksa B, Freiberger D, Liu PL (1985) A clinical sign to predict difficult tracheal intubation: a prospective study. Can Anaesth Soc J 32(4):429–434PubMedCrossRefGoogle Scholar
  7. 7.
    Guillamondegui OD, Gunter OL, Hines L, Martin BJ, Gibson W, Clarke PC, Cecil WT, Cofer JB (2012) Using the national surgical quality improvement program and the tennessee surgical quality collaborative to improve surgical outcomes. J Am Coll Surg 214(4):709–714. doi:10.1016/j.jamcollsurg.2011.12.012 discussion 714–706PubMedCrossRefGoogle Scholar
  8. 8.
    Hall BL, Hamilton BH, Richards K, Bilimoria KY, Cohen ME, Ko CY (2009) Does surgical quality improve in the American College of Surgeons National Surgical Quality Improvement Program: an evaluation of all participating hospitals. Ann Surg 250(3):363–376. doi:10.1097/SLA.0b013e3181b4148f PubMedGoogle Scholar
  9. 9.
    Ingraham AM, Richards KE, Hall BL, Ko CY (2010) Quality improvement in surgery: the American College of Surgeons National Surgical Quality Improvement Program approach. Adv Surg 44:251–267PubMedCrossRefGoogle Scholar
  10. 10.
    Wong JM, Panchmatia JR, Ziewacz JE, Bader AM, Dunn IF, Laws ER, Gawande AA (2012) Patterns in neurosurgical adverse events: intracranial neoplasm surgery. Neurosurg Focus 33(5):E16. doi:10.3171/2012.7.FOCUS12183 PubMedCrossRefGoogle Scholar
  11. 11.
    Fadul CWJ, Thaler H, Galicich J, Patterson RH, Posner JB (1988) Morbidity and mortality of craniotomy for excision of supratentorial gliomas. Neurology 38:1374–1379PubMedCrossRefGoogle Scholar
  12. 12.
    Altshuler EMH, Selker RG, Vertosick FT (1990) The risk and efficacy of anticoagulant therapy in the treatment of thromboembolic complications in patients with primary malignant brain tumors. Neurosurgery 27(1):74–77CrossRefGoogle Scholar
  13. 13.
    Levi ADOWM, Bernstein M, Walters BC (1991) Venous thromboembolism after brain tumor surgery: a retrospective review. Neurosurgery 28:859–863PubMedCrossRefGoogle Scholar
  14. 14.
    Muchmore JHDJ, Culicchia F, Kersten MD (1989) Deep vein thrombophlebitis and pulmonary embolism in patients with malignant gliomas. South Med J 82(11):1352–1356PubMedCrossRefGoogle Scholar
  15. 15.
    Sawaya RG-GP (1992) Postoperative venous thromboembolism and brain tumors: part II. Hemostatic profile. J Neurooncol 14:127–134PubMedGoogle Scholar
  16. 16.
    Sawaya RHR (1992) Postoperative venous thromboembolism and brain tumors: part III. Biochemical profile. J Neurooncol 14:113–118PubMedGoogle Scholar
  17. 17.
    Sawaya RKP (1987) Brain tumors and thromboembolic complications. Surg Neurol 28(2):163PubMedCrossRefGoogle Scholar
  18. 18.
    Sawaya RZM, Elkalliny M, Nishiyama H (1992) Postoperative venous thromboembolism and brain tumors: part I. Clinical profile. J Neurooncol 14:119–125PubMedGoogle Scholar
  19. 19.
    Gross FB Jr, Jaehning DG, Coker WG (1951) The association of migratory thrombophlebitis with carcinoma. N C Med J 12(3):97–101PubMedGoogle Scholar
  20. 20.
    Khorana A (2011) Risk assessment and prophylaxis for VTE in cancer patients. J Nat Compr Canc Netw 9:789–797Google Scholar
  21. 21.
    Marras LC, Geerts WH, Perry JR (2000) The risk of venous thromboembolism is increased throughout the course of malignant glioma: an evidence-based review. Cancer 89(3):640–646PubMedCrossRefGoogle Scholar
  22. 22.
    Khaldi A, Helo N, Schneck MJ, Origitano TC (2011) Venous thromboembolism: deep venous thrombosis and pulmonary embolism in a neurosurgical population. J Neurosurg 114(1):40–46. doi:10.3171/2010.8.JNS10332 PubMedCrossRefGoogle Scholar
  23. 23.
    Poredos P, Jezovnik MK (2007) The role of inflammation in venous thromboembolism and the link between arterial and venous thrombosis. Int Angiol J Int Union Angiol 26(4):306–311Google Scholar
  24. 24.
    Sveinsdottir SV, Svensson PJ, Engstrom G (2013) Inflammatory plasma markers and risk for venous thromboembolism. J Thromb Thrombolysis. doi:10.1007/s11239-013-1033-6 PubMedGoogle Scholar
  25. 25.
    Barnett HGCJ, Llewellyn RC (1977) Safety of mini-dose heparin adminstration for neurosurgical patients. J Neurosurg 47:27–30PubMedCrossRefGoogle Scholar
  26. 26.
    Cerrato D, Ariano C, Fiacchino F (1978) Deep vein thrombosis and low-dose heparin prophylaxis in neurosurgical patients. J Neurosurg 49(3):378–381. doi:10.3171/jns.1978.49.3.0378 PubMedCrossRefGoogle Scholar
  27. 27.
    Frim DM, Barker FG, 2nd, Poletti CE, Hamilton AJ (1992) Postoperative low-dose heparin decreases thromboembolic complications in neurosurgical patients. Neurosurgery 30(6):830–832 discussion 832-833PubMedCrossRefGoogle Scholar
  28. 28.
    Gerlach R, Scheuer T, Beck J, Woszczyk A, Seifert V, Raabe A (2003) Risk of postoperative hemorrhage after intracranial surgery after early nadroparin administration: results of a prospective study. Neurosurgery 53(5):1028–1034 discussion 1034-1025PubMedCrossRefGoogle Scholar
  29. 29.
    Macdonald RL, Amidei C, Baron J, Weir B, Brown F, Erickson RK, Hekmatpanah J, Frim D (2003) 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 59(5):363–372 discussion 372-364PubMedCrossRefGoogle Scholar
  30. 30.
    Raabe A, Gerlach R, Zimmermann M, Seifert V (2001) The risk of haemorrhage associated with early postoperative heparin administration after intracranial surgery. Acta Neurochir (Wien) 143(1):1–7CrossRefGoogle Scholar
  31. 31.
    Goldhaber SZ, Dunn K, Gerhard-Herman M, Park JK, Black PM (2002) Low rate of venous thromboembolism after craniotomy for brain tumor using multimodality prophylaxis. Chest 122(6):1933–1937PubMedCrossRefGoogle Scholar
  32. 32.
    Danish SF, Burnett MG, Ong JG, Sonnad SS, Maloney-Wilensky E, Stein SC (2005) Prophylaxis for deep venous thrombosis in craniotomy patients: a decision analysis. Neurosurgery 56(6):1286–1292 discussion 1292–1284PubMedCrossRefGoogle Scholar
  33. 33.
    Perry JR, Julian JA, Laperriere NJ, Geerts W, Agnelli G, Rogers LR, Malkin MG, Sawaya R, Baker R, Falanga A, Parpia S, Finch T, Levine MN (2010) PRODIGE: a randomized placebo-controlled trial of dalteparin low-molecular-weight heparin thromboprophylaxis in patients with newly diagnosed malignant glioma. J Thromb Haemost JTH 8(9):1959–1965. doi:10.1111/j.1538-7836.2010.03973.x CrossRefGoogle Scholar
  34. 34.
    Constantini S, Kanner A, Friedman A, Shoshan Y, Israel Z, Ashkenazi E, Gertel M, Even A, Shevach Y, Shalit M, Umansky F, Rappaport ZH (2001) Safety of perioperative minidose heparin in patients undergoing brain tumor surgery: a prospective, randomized, double-blind study. J Neurosurg 94(6):918–921. doi:10.3171/jns.2001.94.6.0918 PubMedCrossRefGoogle Scholar
  35. 35.
    Melon E, Keravel Y, Gaston A (1991) NEUOONOX group. Deep venous thrombosis prophylaxis by low molecular weight heparin in neurosurgical patients. Anesthesiology 75:A214CrossRefGoogle Scholar
  36. 36.
    Dickinson LD, Miller LD, Patel CP, Gupta SK (1998) Enoxaparin increases the incidence of postoperative intracranial hemorrhage when initiated preoperatively for deep venous thrombosis prophylaxis in patients with brain tumors. Neurosurgery 43(5):1074–1081PubMedCrossRefGoogle Scholar
  37. 37.
    Agnelli G, Piovella F, Buoncristiani P, Severi P, Pini M, D’Angelo A, Beltrametti C, Damiani M, Andrioli GC, Pugliese R, Iorio A, Brambilla G (1998) Enoxaparin plus compression stockings compared with compression stockings alone in the prevention of venous thromboembolism after elective neurosurgery. N Engl J Med 339(2):80–85. doi:10.1056/NEJM199807093390204 PubMedCrossRefGoogle Scholar
  38. 38.
    Patel AP, Koltz MT, Sansur CA, Gulati M, Hamilton DK (2013) An analysis of deep vein thrombosis in 1,277 consecutive neurosurgical patients undergoing routine weekly ultrasonography. J Neurosurg 118(3):505–509. doi:10.3171/2012.11.JNS121243 PubMedCrossRefGoogle Scholar
  39. 39.
    Palareti G (2014) How I treat isolated distal deep vein thrombosis (IDDVT). Blood. doi:10.1182/blood-2013-10-512616 Google Scholar
  40. 40.
    Palareti G, Schellong S (2012) Isolated distal deep vein thrombosis: what we know and what we are doing. J Thromb Haemost JTH 10(1):11–19. doi:10.1111/j.1538-7836.2011.04564.x CrossRefGoogle Scholar
  41. 41.
    Hamada K, Kuratsu J, Saitoh Y, Takeshima H, Nishi T, Ushio Y (1996) Expression of tissue factor correlates with grade of malignancy in human glioma. Cancer 77(9):1877–1883. doi:10.1002/(SICI)1097-0142(19960501)77:9<1877:AID-CNCR18>3.0.CO;2-X PubMedCrossRefGoogle Scholar
  42. 42.
    Rodas RA, Fenstermaker RA, McKeever PE, Blaivas M, Dickinson LD, Papadopoulos SM, Hoff JT, Hopkins LN, Duffy-Fronckowiak M, Greenberg HS (1998) Correlation of intraluminal thrombosis in brain tumor vessels with postoperative thrombotic complications: a preliminary report. J Neurosurg 89(2):200–205. doi:10.3171/jns.1998.89.2.0200 PubMedCrossRefGoogle Scholar
  43. 43.
    Hawn MT, Vick CC, Richman J, Holman W, Deierhoi RJ, Graham LA, Henderson WG, Itani KM (2011) Surgical site infection prevention: time to move beyond the surgical care improvement program. Ann Surg 254(3):494–499. doi:10.1097/SLA.0b013e31822c6929 discussion 499-501PubMedCrossRefGoogle Scholar
  44. 44.
    Rasouli MR, Jaberi MM, Hozack WJ, Parvizi J, Rothman RH (2013) Surgical care improvement project (SCIP): has its mission succeeded? J Arthroplasty 28(7):1072–1075. doi:10.1016/j.arth.2013.03.004 PubMedCrossRefGoogle Scholar
  45. 45.
    Wang Y, Eldridge N, Metersky ML, Verzier NR, Meehan TP, Pandolfi MM, Foody JM, Ho SY, Galusha D, Kliman RE, Sonnenfeld N, Krumholz HM, Battles J (2014) National trends in patient safety for four common conditions, 2005-2011. N Engl J Med 370(4):341–351. doi:10.1056/NEJMsa1300991 PubMedCentralPubMedCrossRefGoogle Scholar
  46. 46.
    Bilimoria KY, Chung J, Ju MH, Haut ER, Bentrem DJ, Ko CY, Baker DW (2013) Evaluation of surveillance bias and the validity of the venous thromboembolism quality measure. JAMA J Am Med Assoc 310(14):1482–1489. doi:10.1001/jama.2013.280048 CrossRefGoogle Scholar
  47. 47.
    Bostrom S, Holmgren E, Jonsson O, Lindberg S, Lindstrom B, Winso I, Zachrisson B (1986) 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) 80(3–4):83–89CrossRefGoogle Scholar
  48. 48.
    Nurmohamed MT, Van Riel AM, Henkens CMA, Koopman MMW, Que GTH, d’Azemar P, Buller HR, Ten Cate JW, Hoek JA, van der Meer J, van der Heul C, Turple AGG, Haley S, Haley S, Sicurella A, Gent M (1996) Low molecular weight heparin and compression stockings in the prevention of venous thromboembolism in neurosurgery. Thromb Haemost 75(2):233–238PubMedGoogle Scholar
  49. 49.
    Gould MK, Garcia DA, Wren SM, Karanicolas PJ, Arcelus JI, Heit JA, Samama CM, American College of Chest P (2012) 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 141(2 Suppl):e227S–277S. doi:10.1378/chest.11-2297 PubMedCentralPubMedGoogle Scholar
  50. 50.
    Salmaggi A, Simonetti G, Trevisan E, Beecher D, Carapella CM, DiMeco F, Conti L, Pace A, Filippini G (2013) Perioperative thromboprophylaxis in patients with craniotomy for brain tumours: a systematic review. J Neurooncol 113(2):293–303. doi:10.1007/s11060-013-1115-5 PubMedCrossRefGoogle Scholar
  51. 51.
    Simanek R, Vormittag R, Hassler M, Roessler K, Schwarz M, Zielinski C, Pabinger I, Marosi C (2007) Venous thromboembolism and survival in patients with high-grade glioma. Neuro-oncology 9(2):89–95. doi:10.1215/15228517-2006-035 PubMedCentralPubMedCrossRefGoogle Scholar
  52. 52.
    Chen JY, Hovey E, Rosenthal M, Livingstone A, Simes J (2014) Neuro-oncology practices in Australia: A cooperative group for neuro-oncology patterns of care study. Asia Pac J Clin Oncol 10(2):162–167. doi:10.1111/ajco.12079 PubMedCrossRefGoogle Scholar
  53. 53.
    Collaboration CT, Dennis M, Sandercock P, Reid J, Graham C, Forbes J, Murray G (2013) 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 382(9891):516–524. doi:10.1016/S0140-6736(13)61050-8 CrossRefGoogle Scholar
  54. 54.
    Misra M, Roitberg B, Ebersole K, Charbel FT (2004) Prevention of pulmonary embolism by combined modalities of thromboprophylaxis and intensive surveillance protocol. Neurosurgery 54(5):1099–1102 discussion 1102–1093PubMedCrossRefGoogle Scholar
  55. 55.
    Prell J, Rachinger J, Smaczny R, Taute BM, Rampp S, Illert J, Koman G, Marquart C, Rachinger A, Simmermacher S, Alfieri A, Scheller C, Strauss C (2013) D-dimer plasma level: a reliable marker for venous thromboembolism after elective craniotomy. J Neurosurg 119(5):1340–1346. doi:10.3171/2013.5.JNS13151 PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  1. 1.Department of NeurosurgeryUniversity of Rochester Medical CenterRochesterUSA

Personalised recommendations