Risk of Venous Thromboembolism in Patients with Cancer: A Systematic Review and Meta-Analysis

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Background:
People with cancer are known to be at increased risk of venous thromboembolism (VTE), and this risk is believed to vary according to cancer type, stage of disease, and treatment modality. Our purpose was to summarise the existing literature to determine precisely and accurately the absolute risk of VTE in cancer patients, stratified by malignancy site and background risk of VTE.

Methods and Findings:
We searched the Medline and Embase databases from 1 January 1966 to 14 July 2011 to identify cohort studies comprising people diagnosed with one of eight specified cancer types or where participants were judged to be representative of all people with cancer. For each included study, the number of patients who developed clinically apparent VTE, and the total person-years of follow-up were extracted. Incidence rates of VTE were pooled across studies using the generic inverse variance method. In total, data from 38 individual studies were included. Among average-risk patients, the overall risk of VTE was estimated to be 13 per 1,000 person-years (95% CI, 7 to 23), with the highest risk among patients with cancers of the pancreas, brain, and lung. Among patients judged to be at high risk (due to metastatic disease or receipt of high-risk treatments), the risk of VTE was 68 per 1,000 person-years (95% CI, 48 to 96), with the highest risk among patients with brain cancer (200 per 1,000 person-years; 95% CI, 162 to 247). Our results need to be considered in light of high levels of heterogeneity, which exist due to differences in study population, outcome definition, and average duration of follow-up between studies.

Conclusions:
VTE occurs in greater than 1% of cancer patients each year, but this varies widely by cancer type and time since diagnosis. The absolute VTE risks obtained from this review can aid in clinical decision-making about which people with cancer should receive anticoagulant prophylaxis and at what times.

Please see later in the article for the Editors' Summary.

Vyšlo v časopise: Risk of Venous Thromboembolism in Patients with Cancer: A Systematic Review and Meta-Analysis. PLoS Med 9(7): e32767. doi:10.1371/journal.pmed.1001275
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pmed.1001275

Souhrn

Zdroje

1. HeitJA, CohenAT, AndersonFAJr (2005) on behalf of the VTE Impact Assessment Group (2005) Estimated annual number of incident and recurrent, non-fatal and fatal venous thromboembolism (VTE) events in the US. ASH Annual Meeting Abstracts 106: 910.

2. HeitJA, O'FallonWM, PettersonTM, LohseCM, SilversteinMD, et al. (2002) Relative impact of risk factors for deep vein thrombosis and pulmonary embolism: a population-based study. Arch Intern Med 162: 1245–1248.

3. SorensenHT, MellemkjaerL, OlsenJH, BaronJA (2000) Prognosis of cancers associated with venous thromboembolism. N Engl J Med 343: 1846–1850.

4. KohlerBA, WardE, McCarthyBJ, SchymuraMJ, RiesLAG, et al. (2011) Annual report to the nation on the status of cancer, 1975–2007, featuring tumors of the brain and other nervous system. J Natl Canc Inst 103: 714–736.

5. VincentGK, VelkoffVA (2010) The next four decades—the older population in the United States: 2010 to 2050. Population estimates and projections. Washington (District of Columbia): US Census Bureau.

6. HeitJA, SilversteinMD, MohrDN, PettersonTM, O'FallonWM, et al. (2000) Risk factors for deep vein thrombosis and pulmonary embolism: a population-based case-control study. Arch Intern Med 160: 809–815.

7. WhiteRH, ZhouH, RomanoPS (2003) Incidence of symptomatic venous thromboembolism after different elective or urgent surgical procedures. Thromb Haemost 90: 446–455.

8. KhoranaAA, ConnollyGC (2009) Assessing risk of venous thromboembolism in the patient with cancer. J Clin Oncol 27: 4839–4847.

9. LymanGH, KhoranaAA, FalangaA, Clarke-PearsonD, FlowersC, et al. (2007) American Society of Clinical Oncology guideline: recommendations for venous thromboembolism prophylaxis and treatment in patients with cancer. J Clin Oncol 25: 5490–5505.

10. MandalàM, FalangaA, PiccioliA, PrandoniP, PoglianiEM, et al. (2006) Venous thromboembolism and cancer: guidelines of the Italian Association of Medical Oncology (AIOM). Crit Rev Oncol Hemat 59: 194–204.

11. KahnSR, LimW, DunnAS, CushmanM, DentaliF, et al. (2012) 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 141: e195S–e226S.

12. StreiffMB, BockenstedtPL, CatalandSR, ChesneyC, EbyC, et al. (2011) Venous thromboembolic disease. J Natl Compr Canc Netw 9: 714–777.

13. KhoranaAA, FrancisCW, CulakovaE, KudererNM, LymanGH (2007) Frequency, risk factors, and trends for venous thromboembolism among hospitalized cancer patients. Cancer 110: 2339–2346.

14. LevitanN, DowlatiA, RemickSC, TahsildarHI, SivinskiLD, et al. (1999) Rates of initial and recurrent thromboembolic disease among patients with malignancy versus those without malignancy. Risk analysis using Medicare claims data. Medicine (Baltimore) 78: 285–291.

15. SteinPD, BeemathA, MeyersFA, SkafE, SanchezJ, et al. (2006) Incidence of venous thromboembolism in patients hospitalized with cancer. Am J Med 119: 60–68.

16. MoherD, LiberatiA, TetzlaffJ, AltmanDG, ThePG (2009) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med 6: e1000097 doi:10.1371/journal.pmed.1000097.

17. SatarianoWA, SillimanRA (2003) Comorbidity: implications for research and practice in geriatric oncology. Crit Rev Oncol Hemat 48: 239–248.

18. Cancer Research UK (2012) January 27 Cancer incidence—UK statistics [database]. Available: http://info.cancerresearchuk.org/cancerstats/incidence/. Accessed 28 March 2012.

19. KhoranaAA, FrancisCW, CulakovaE, LymanGH (2005) Risk factors for chemotherapy-associated venous thromboembolism in a prospective observational study. Cancer 104: 2822–2829.

20. AyC, VormittagR, DunklerD, SimanekR, ChiriacA-L, et al. (2009) D-dimer and prothrombin fragment 1+2 predict venous thromboembolism in patients with cancer: results from the Vienna Cancer and Thrombosis Study. J Clin Oncol 27: 4124–4129.

21. SuttonAJ, AbramsKR, JonesDR, SheldonTA, SongF (2000) Methods for meta-analysis in medical research. Chichester (United Kingdom): Wiley.

22. HigginsJPT, ThompsonSG, DeeksJJ, AltmanDG (2003) Measuring inconsistency in meta-analyses. BMJ 327: 557–560.

23. Abdel-RazeqHN, HijjawiSB, JalladSG, AbabnehBA (2010) Venous thromboembolism risk stratification in medically-ill hospitalized cancer patients. A comprehensive cancer center experience. J Thromb Thrombolysis 30: 286–293.

24. AlcalayA, WunT, KhatriV, ChewHK, HarveyD, et al. (2006) Venous thromboembolism in patients with colorectal cancer: incidence and effect on survival. J Clin Oncol 24: 1112–1118.

25. AndtbackaRHI, BabieraG, SingletarySE, HuntKK, Meric-BernstamF, et al. (2006) Incidence and prevention of venous thromboembolism in patients undergoing breast cancer surgery and treated according to clinical pathways. Ann Surg 243: 96–101.

26. AraiY, EgawaS, TobisuK, SagiyamaK, SumiyoshiY, et al. (2000) Radical retropubic prostatectomy: time trends, morbidity and mortality in Japan. BJU Int 85: 287–294.

27. AugusteKI, Quinones-HinojosaA, GadkaryC, ZadaG, LambornKR, et al. (2003) Incidence of venous thromboembolism in patients undergoing craniotomy and motor mapping for glioma without intraoperative mechanical prophylaxis to the contralateral leg. J Neurosurg 99: 680–684.

28. BlomJW, OsantoS, RosendaalFR (2004) The risk of a venous thrombotic event in lung cancer patients: higher risk for adenocarcinoma than squamous cell carcinoma. J Thromb Haemost 2: 1760–1765.

29. BlomJW, OsantoS, RosendaalFR (2006) High risk of venous thrombosis in patients with pancreatic cancer: a cohort study of 202 patients. Eur J Cancer 42: 410–414.

30. BlomJW, VanderschootJPM, OostindierMJ, OsantoS, van der MeerFJM, et al. (2006) Incidence of venous thrombosis in a large cohort of 66,329 cancer patients: results of a record linkage study. J Thromb Haemost 4: 529–535.

31. BrandesAA, ScelziE, SalmistraroG, ErmaniM, CarolloC, et al. (1997) Incidence of risk of thromboembolism during treatment of high-grade gliomas: a prospective study. Eur J Cancer 33: 1592–1596.

32. ChewHK, DaviesAM, WunT, HarveyD, ZhouH, et al. (2008) The incidence of venous thromboembolism among patients with primary lung cancer. J Thromb Haemost 6: 601–608.

33. ChewHK, WunT, HarveyD, ZhouH, WhiteRH (2006) Incidence of venous thromboembolism and its effect on survival among patients with common cancers. Arch Intern Med 166: 458–464.

34. ChewHK, WunT, HarveyDJ, ZhouH, WhiteRH (2007) Incidence of venous thromboembolism and the impact on survival in breast cancer patients. J Clin Oncol 25: 70–76.

35. ConnollyGC, KhoranaAA, KudererNM, CulakovaE, FrancisCW, et al. (2010) Leukocytosis, thrombosis and early mortality in cancer patients initiating chemotherapy. Thromb Res 126: 113–118.

36. Cronin-FentonDP, SondergaardF, PedersenLA, FryzekJP, CetinK, et al. (2010) Hospitalisation for venous thromboembolism in cancer patients and the general population: a population-based cohort study in Denmark, 1997–2006. Br J Cancer 103: 947–953.

37. De StefanoV, SoraF, RossiE, ChiusoloP, LaurentiL, et al. (2005) The risk of thrombosis in patients with acute leukemia: occurrence of thrombosis at diagnosis and during treatment. J Thromb Haemost 3: 1985–1992.

38. Di NisioM, FerranteN, De TursiM, IacobelliS, CuccurulloF, et al. (2010) Incidental venous thromboembolism in ambulatory cancer patients receiving chemotherapy. Thromb Haemost 104: 1049–1054.

39. HallIE, AndersenMS, KrumholzHM, GrossCP (2009) Predictors of venous thromboembolism in patients with advanced common solid cancers. J Cancer Epidemiol 2009: 182521 doi:10.1155/2009/182521.

40. HernandezRK, SorensenHT, PedersenL, JacobsenJ, LashTL (2009) Tamoxifen treatment and risk of deep venous thrombosis and pulmonary embolism: a Danish population-based cohort study. Cancer 115: 4442–4449.

41. KanzR, VukovichT, VormittagR, DunklerD, AyC, et al. (2011) Thrombosis risk and survival in cancer patients with elevated C-reactive protein. J Thromb Haemost 9: 57–63.

42. KaufmanJL, NookaA, VranaM, GleasonC, HeffnerLT, et al. (2010) Bortezomib, thalidomide, and dexamethasone as induction therapy for patients with symptomatic multiple myeloma: a retrospective study. Cancer 116: 3143–3151.

43. KirwanCC, McDowellG, McCollumCN, KumarS, ByrneGJ (2008) Early changes in the haemostatic and procoagulant systems after chemotherapy for breast cancer. Br J Cancer 99: 1000–1006.

44. KomrokjiRS, UppalNP, KhoranaAA, LymanGH, KaplanKL, et al. (2006) Venous thromboembolism in patients with diffuse large B-cell lymphoma. Leuk Lymphoma 47: 1029–1033.

45. KuGH, WhiteRH, ChewHK, HarveyDJ, ZhouH, et al. (2009) Venous thromboembolism in patients with acute leukemia: incidence, risk factors, and effect on survival. Blood 113: 3911–3917.

46. MandalaM, BarniS, PrinsM, LabiancaR, TondiniC, et al. (2010) Acquired and inherited risk factors for developing venous thromboembolism in cancer patients receiving adjuvant chemotherapy: a prospective trial. Ann Oncol 21: 871–876.

47. MasonDP, QuaderMA, BlackstoneEH, RajeswaranJ, DeCampMM, et al. (2006) Thromboembolism after pneumonectomy for malignancy: an independent marker of poor outcome. J Thorac Cardiovasc Surg 131: 711–718.

48. NegaardHFS, IversenPO, OstenstadB, IversenN, HolmePA, et al. (2008) Hypercoagulability in patients with haematological neoplasia: no apparent initiation by tissue factor. Thromb Haemost 99: 1040–1048.

49. NumicoG, GarroneO, DongiovanniV, SilvestrisN, ColantonioI, et al. (2005) Prospective evaluation of major vascular events in patients with nonsmall cell lung carcinoma treated with cisplatin and gemcitabine. Cancer 103: 994–999.

50. OhSY, KimJH, LeeK-W, BangS-M, HwangJ-H, et al. (2008) Venous thromboembolism in patients with pancreatic adenocarcinoma: lower incidence in Asian ethnicity. Thromb Res 122: 485–490.

51. OttenH-MMB, MathijssenJ, ten CateH, SoesanM, InghelsM, et al. (2004) Symptomatic venous thromboembolism in cancer patients treated with chemotherapy: an underestimated phenomenon. Arch Intern Med 164: 190–194.

52. PorukKE, FirpoMA, HuerterLM, ScaifeCL, EmersonLL, et al. (2010) Serum platelet factor 4 is an independent predictor of survival and venous thromboembolism in patients with pancreatic adenocarcinoma. Cancer Epidemiol Biomarkers Prev 19: 2605–2610.

53. ReevesD, LiuCY (2010) Retrospective evaluation of venous thromboembolism prophylaxis in the adult cancer population. J Oncol Pharm Pract 16: 27–31.

54. SallahS, WanJY, NguyenNP (2002) Venous thrombosis in patients with solid tumors: determination of frequency and characteristics. Thromb Haemost 87: 575–579.

55. SecinFP, JibornT, BjartellAS, FournierG, SalomonL, et al. (2008) Multi-institutional study of symptomatic deep venous thrombosis and pulmonary embolism in prostate cancer patients undergoing laparoscopic or robot-assisted laparoscopic radical prostatectomy. Eur Urol 53: 134–145.

56. SemradTJ, O'DonnellR, WunT, ChewH, HarveyD, et al. (2007) Epidemiology of venous thromboembolism in 9489 patients with malignant glioma. J Neurosurg 106: 601–608.

57. SgarabottoD, PrandoniP, StefaniPM, ScanoF, VianelloF, et al. (1998) Prevalence and patterns of symptomatic thromboembolism in oncohematology. Haematologica 83: 442–446.

58. SimanekR, VormittagR, HasslerM, RoesslerK, SchwarzM, et al. (2007) Venous thromboembolism and survival in patients with high-grade glioma. Neuro Oncol 9: 89–95.

59. StreiffMB, SegalJ, GrossmanSA, KicklerTS, WeirEG (2004) ABO blood group is a potent risk factor for venous thromboembolism in patients with malignant gliomas. Cancer 100: 1717–1723.

60. TagalakisV, LeviD, AgulnikJS, CohenV, KasymjanovaG, et al. (2007) High risk of deep vein thrombosis in patients with non-small cell lung cancer: a cohort study of 493 patients. J Thorac Oncol 2: 729–734.

61. Van HemelrijckM, AdolfssonJ, GarmoH, Bill-AxelsonA, BrattO, et al. (2010) Risk of thromboembolic diseases in men with prostate cancer: results from the population-based PCBaSe Sweden. Lancet Oncol 11: 450–458.

62. VormittagR, SimanekR, AyC, DunklerD, QuehenbergerP, et al. (2009) High factor VIII levels independently predict venous thromboembolism in cancer patients: the cancer and thrombosis study. Arterioscler Thromb Vasc Biol 29: 2176–2181.

63. WederW, CollaudS, EberhardtWEE, HillingerS, WelterS, et al. (2010) Pneumonectomy is a valuable treatment option after neoadjuvant therapy for stage III non-small-cell lung cancer. J Thorac Cardiovasc Surg 139: 1424–1430.

64. WhittleAM, AllsupDJ, BaileyJR (2011) Chronic lymphocytic leukaemia is a risk factor for venous thromboembolism. Leuk Res 35: 419–421.

65. ZecchinaG, GhioP, BosioS, CravinoM, CamaschellaC, et al. (2007) Reactive thrombocytosis might contribute to chemotherapy-related thrombophilia in patients with lung cancer. Clin Lung Cancer 8: 264–267.

66. ZhouX, TeegalaS, HuenA, JiY, FayadL, et al. (2010) Incidence and risk factors of venous thromboembolic events in lymphoma. Am J Med 123: 935–941.

67. CherukuR, TapazoglouE, EnsleyJ, KishJA, CummingsGD, et al. (1991) The incidence and significance of thromboembolic complications in patients with high-grade gliomas. Cancer 68: 2621–2624.

68. ClarkeCS, OtridgeBW, CarneyDN (1990) Thromboembolism. A complication of weekly chemotherapy in the treatment of non-Hodgkin's lymphoma. Cancer 66: 2027–2030.

69. DentaliF, MalatoA, AgenoW, ImperatoriA, CajozzoM, et al. (2008) Incidence of venous thromboembolism in patients undergoing thoracotomy for lung cancer. J Thorac Cardiovasc Surg 135: 705–706.

70. DhamiMS, BonaRD, CalogeroJA, HellmanRM (1993) Venous thromboembolism and high grade gliomas. Thromb Haemost 70: 393–396.

71. HershmanDL, BuonoDL, MalinJ, McBrideR, TsaiWY, et al. (2009) Patterns of use and risks associated with erythropoiesis-stimulating agents among Medicare patients with cancer. J Natl Cancer Inst 101: 1633–1641.

72. HoyJ, NeemanT, Stuart-HarrisR, DavisA (2009) Risk of venous thromboembolism in patients receiving adjuvant chemotherapy with 5-fluorouracil, epirubicin and cyclophosphamide for early breast cancer. Asia Pac J Clin Oncol 5: 129–136.

73. ImbertiD, VallisaD, AnselmiE, MoroniCF, BerteR, et al. (2004) Safety and efficacy of enoxaparin treatment in venous thromboembolic disease during acute leukemia. Tumori 90: 390–393.

74. IversenLH, OkholmM, Thorlacius-UssingO (1996) Pre- and postoperative state of coagulation and fibrinolysis in plasma of patients with benign and malignant colorectal disease—a preliminary study. Thromb Haemost 76: 523–528.

75. LernerSE, BluteML, LieberMM, ZinckeH (1995) Morbidity of contemporary radical retropubic prostatectomy for localized prostate cancer. Oncology (Williston) 9: 379–389.

76. MandalaM, FalangaA, CremonesiM, ZaccanelliM, FlorianiI, et al. (2006) The extension of disease is associated to an increased risk of venous thromboembolism (VTE) in patients with gastrointestinal (GI) carcinoma. Thromb Haemost 95: 752–754.

77. MitchellSY, LingardEA, KestevenP, McCaskieAW, GerrandCH (2007) Venous thromboembolism in patients with primary bone or soft-tissue sarcomas. J Bone Joint Surg Am 89: 2433–2439.

78. RoddyJVF, PartridgeSM, RockeyML, PruemerJM, GuoJJ, et al. (2010) Thromboembolic events in patients with colorectal cancer receiving the combination of bevacizumab-based chemotherapy and erythropoietin stimulating agents. Am J Clin Oncol 33: 36–42.

79. RuggieriP, MontaltiM, PalaE, AngeliniA, CalabroT, et al. (2010) Clinically significant thromboembolic disease in orthopedic oncology: an analysis of 986 patients treated with low-molecular-weight heparin. J Surg Oncol 102: 375–379.

80. SantosFPS, AlvaradoY, KantarjianH, VermaD, O'BrienS, et al. (2011) Long-term prognostic impact of the use of erythropoietic-stimulating agents in patients with chronic myeloid leukemia in chronic phase treated with imatinib. Cancer 117: 982–991.

81. SeifterEJ, YoungRC, LongoDL (1985) Deep venous thrombosis during therapy for Hodgkin's disease. Cancer Treat Rep 69: 1011–1013.

82. SilvaniA, SalmaggiA, EoliM, LampertiE, BoiardiA (2003) Venous thromboembolism in malignant glioma patients treated by chemoradiotherapy. Neurol Sci 24: 272.

83. ZinckeH, OesterlingJE, BluteML, BergstralhEJ, MyersRP, et al. (1994) Long-term (15 years) results after radical prostatectomy for clinically localized (stage T2c or lower) prostate cancer. J Urol 152: 1850–1857.

84. RodriguesC, FerrarottoR, FilhoR, NovisY, HoffP (2010) Venous thromboembolism and cancer: a systematic review. J Thromb Thrombolysis 30: 67–78.

85. EadenJA, AbramsKR, MayberryJF (2001) The risk of colorectal cancer in ulcerative colitis: a meta-analysis. Gut 48: 526–535.

86. ThomasT, AbramsKA, RobinsonRJ, MayberryJF (2007) Meta-analysis: cancer risk of low-grade dysplasia in chronic ulcerative colitis. Alimen Pharm Ther 25: 657–668.

87. BlomJW, DoggenCJM, OsantoS, RosendaalFR (2005) Malignancies, prothrombotic mutations, and the risk of venous thrombosis. JAMA 293: 715–722.

88. CohenAT, DavidsonBL, GallusAS, LassenMR, PrinsMH, et al. (2006) Efficacy and safety of fondaparinux for the prevention of venous thromboembolism in older acute medical patients: randomised placebo controlled trial. BMJ 332: 325–329.

89. MismettiP, Laporte-SimitsidisS, TardyB, CucheratM, BuchmullerA, et al. (2000) Prevention of venous thromboembolism in internal medicine with unfractionated or low-molecular-weight heparins: a meta-analysis of randomised clinical trials. Thromb Haemost 83: 14–19.

90. LevineM, HirshJ, GentM, ArnoldA, WarrD, et al. (1994) Double-blind randomized trial of very-low-dose warfarin for prevention of thromboembolism in stage-IV breast-cancer. Lancet 343: 886–889.

91. MeyerG, MarjanovicZ, ValckeJ, LorcerieB, GruelY, et al. (2002) Comparison of low-molecular-weight heparin and warfarin for the secondary prevention of venous thromboembolism in patients with cancer: a randomized controlled study. Arch Intern Med 162: 1729–1735.

92. PrandoniP, LensingAWA, PiccioliA, BernardiE, SimioniP, et al. (2002) Recurrent venous thromboembolism and bleeding complications during anticoagulant treatment in patients with cancer and venous thrombosis. Blood 100: 3484–3488.