Download PDF
Thromb Haemost 2012; 108(02): 225-235
DOI: 10.1160/TH12-01-0010
Blood Coagulation, Fibrinolysis and Cellular Haemostasis
Schattauer GmbH

A nation-wide analysis of venous thromboembolism in 497,180 cancer patients with the development and validation of a risk-stratification scoring system

Yuan-Bin Yu   *
1   Institutes of Physiology, School of Medicine, National Yang-Ming University, Taipei, Taiwan
2   Faculty of Medicine, School of Medicine, National Yang-Ming University, Taipei, Taiwan
4   Division of Hematology and Oncology, Department of Medicine, Taipei Veterans General Hospital, Taipei, Taiwan
,
Jyh-Pyng Gau   *
2   Faculty of Medicine, School of Medicine, National Yang-Ming University, Taipei, Taiwan
4   Division of Hematology and Oncology, Department of Medicine, Taipei Veterans General Hospital, Taipei, Taiwan
,
Chun-Yu Liu
2   Faculty of Medicine, School of Medicine, National Yang-Ming University, Taipei, Taiwan
4   Division of Hematology and Oncology, Department of Medicine, Taipei Veterans General Hospital, Taipei, Taiwan
,
Muh-Hwa Yang
2   Faculty of Medicine, School of Medicine, National Yang-Ming University, Taipei, Taiwan
4   Division of Hematology and Oncology, Department of Medicine, Taipei Veterans General Hospital, Taipei, Taiwan
,
Shu-Chiung Chiang
5   Information Management Office, Taipei Veterans General Hospital, Taipei, Taiwan
,
Hui-Chi Hsu
1   Institutes of Physiology, School of Medicine, National Yang-Ming University, Taipei, Taiwan
2   Faculty of Medicine, School of Medicine, National Yang-Ming University, Taipei, Taiwan
4   Division of Hematology and Oncology, Department of Medicine, Taipei Veterans General Hospital, Taipei, Taiwan
,
Ying-Chung Hong
2   Faculty of Medicine, School of Medicine, National Yang-Ming University, Taipei, Taiwan
4   Division of Hematology and Oncology, Department of Medicine, Taipei Veterans General Hospital, Taipei, Taiwan
,
Liang-Tsai Hsiao
2   Faculty of Medicine, School of Medicine, National Yang-Ming University, Taipei, Taiwan
4   Division of Hematology and Oncology, Department of Medicine, Taipei Veterans General Hospital, Taipei, Taiwan
,
Jin-Hwang Liu
2   Faculty of Medicine, School of Medicine, National Yang-Ming University, Taipei, Taiwan
4   Division of Hematology and Oncology, Department of Medicine, Taipei Veterans General Hospital, Taipei, Taiwan
,
Tzeon-Jye Chiou
2   Faculty of Medicine, School of Medicine, National Yang-Ming University, Taipei, Taiwan
4   Division of Hematology and Oncology, Department of Medicine, Taipei Veterans General Hospital, Taipei, Taiwan
,
Po-Min Chen
2   Faculty of Medicine, School of Medicine, National Yang-Ming University, Taipei, Taiwan
4   Division of Hematology and Oncology, Department of Medicine, Taipei Veterans General Hospital, Taipei, Taiwan
,
Tzong-Shyuan Lee
1   Institutes of Physiology, School of Medicine, National Yang-Ming University, Taipei, Taiwan
2   Faculty of Medicine, School of Medicine, National Yang-Ming University, Taipei, Taiwan
,
Li-Fang Chou
7   Department of Public Finance, National Chengchi University, Taipei, Taiwan
,
Cheng-Hwai Tzeng
2   Faculty of Medicine, School of Medicine, National Yang-Ming University, Taipei, Taiwan
4   Division of Hematology and Oncology, Department of Medicine, Taipei Veterans General Hospital, Taipei, Taiwan
,
Tzeng-Ji Chen
2   Faculty of Medicine, School of Medicine, National Yang-Ming University, Taipei, Taiwan
3   Hospital and Health Care Administration, School of Medicine, National Yang-Ming University, Taipei, Taiwan
6   Department of Family Medicine, Taipei Veterans General Hospital, Taipei, Taiwan
› Author Affiliations Financial support: This work was supported by grants from National Science Council Grant No. NSC 98–2410-H-010–003-MY2 & NSC 96–2416-H-004–007-MY2, Taipei Veterans Gener Hospital Grant No. V97A-113 & V98B1–011, and Taiwan Clinical Oncology Research Foundation.
Further Information

Publication History

Received: 10 January 2012

Accepted after major revision: 12 April 2012

Publication Date:
25 November 2017 (online)

    Permissions and Reprints

Summary

The Asian population is thought to have a low risk of venous thromboembolism (VTE), but the epidemiology of VTE in cancer patients remains unclear. The National Health Insurance Research Database of Taiwan was used to find hospitalised patients newly-diagnosed with cancer to determine the incidence of VTE in cancer patients and to identify the risk factors for VTE. Between 1997 and 2005, 497,180 cancer patients were identified. During a median follow-up of 21.3 months (range 0–119.9 months), 5,296 patients developed VTE. The estimated incidence was 185 events per 100,000 person-years. Patients with a prior history of VTE and female patients between the ages of 40 and 80 carried high risk of VTE. The rate of VTE was relatively high in patients with myeloma, prostate cancer, lung cancer, gynaecologic cancers, sarcoma, and metastasis of unknown origin. We developed a risk-stratification scoring system to divide the cancer patients into four discrete risk groups (very low risk, low risk, intermediate, and high risk). The incidence of VTE in each group was 0.5%, 0.9%, 1.5%, and 8.7%, respectively (p < 0.001). This scoring system was validated in a separate patient cohort. In conclusion, VTE is a distinct burden for cancer patients in Taiwan. The risk scoring system could prove helpful in decision-making concerning thromboprophylaxis in cancer patients.

Note: The results of this paper were presented as an Asian-Pacific Scholarship Award at the 23rd Congress of the International Society on Thrombosis and Haemostasis, Kyoto, Japan, 23–28 July 2011.

Keywords

Cancer - epidemiology - scoring system - venous thromboembolism

* Y-B. Yu and J-P. Gau contributed equally to this work.


 

  • References

  • 1 Heit JA, O'Fallon WM, Petterson TM. et al. Relative impact of risk factors for deep vein thrombosis and pulmonary embolism: a population-based study. Arch Intern Med 2002; 162: 1245-1248.
    CrossrefPubMedGoogle Scholar
  • 2 Blom JW, Doggen CJ, Osanto S. et al. Malignancies, prothrombotic mutations, and the risk of venous thrombosis. J Am Med Assoc 2005; 293: 715-722.
    CrossrefPubMedGoogle Scholar
  • 3 Stein PD, Beemath A, Meyers FA. et al. Incidence of venous thromboembolism in patients hospitalized with cancer. Am J Med 2006; 119: 60-68.
    CrossrefPubMedGoogle Scholar
  • 4 Gomes MP, Deitcher SR. Diagnosis of venous thromboembolic disease in cancer patients. Oncology (Williston Park) 2003; 17 126-135 139-144.
    PubMedGoogle Scholar
  • 5 Ogren M, Bergqvist D, Wahlander K. et al. Trousseau's syndrome - what is the evidence? A population-based autopsy study. Thromb Haemost 2006; 95: 541-545.
    Article in Thieme ConnectPubMedGoogle Scholar
  • 6 Sallah S, Wan JY, Nguyen NP. Venous thrombosis in patients with solid tumors: determination of frequency and characteristics. Thromb Haemost 2002; 87: 575-579.
    Article in Thieme ConnectPubMedGoogle Scholar
  • 7 Thodiyil PA, Kakkar AK. Variation in relative risk of venous thromboembolism in different cancers. Thromb Haemost 2002; 87: 1076-1077.
    Article in Thieme ConnectPubMedGoogle Scholar
  • 8 Ng HJ, Lee LH. Trends in prevalence of deep venous thrombosis among hospitalised patients in an Asian institution. Thromb Haemost 2009; 101: 1095-1099.
    Article in Thieme ConnectPubMedGoogle Scholar
  • 9 White RH, Zhou H, Romano PS. Incidence of idiopathic deep venous thrombosis and secondary thromboembolism among ethnic groups in California. Ann Intern Med 1998; 128: 737-740.
    CrossrefPubMedGoogle Scholar
  • 10 Klatsky AL, Armstrong MA, Poggi J. Risk of pulmonary embolism and/or deep venous thrombosis in Asian-Americans. Am J Cardiol 2000; 85: 1334-1337.
    CrossrefPubMedGoogle Scholar
  • 11 Stein PD, Kayali F, Olson RE. et al. Pulmonary thromboembolism in Asians/ Pacific Islanders in the United States: analysis of data from the National Hospital Discharge Survey and the United States Bureau of the Census. Am J Med 2004; 116: 435-442.
    CrossrefPubMedGoogle Scholar
  • 12 Mannucci PM. Thrombosis and bleeding disorders outside Western countries. J Thromb Haemost 2007; 5 (Suppl. 01) 68-72.
    CrossrefPubMedGoogle Scholar
  • 13 Lee CH, Lin LJ, Cheng CL. et al. Incidence and cumulative recurrence rates of venous thromboembolism in the Taiwanese population. J Thromb Haemost 2010; 8: 1515-1523.
    CrossrefPubMedGoogle Scholar
  • 14 Chew HK, Wun T, Harvey D. et al. Incidence of venous thromboembolism and its effect on survival among patients with common cancers. Arch Intern Med 2006; 166: 458-464.
    CrossrefPubMedGoogle Scholar
  • 15 Ho CH, Chau WK, Hsu HC. et al. Causes of venous thrombosis in fifty Chinese patients. Am J Hematol 2000; 63: 74-78.
    CrossrefPubMedGoogle Scholar
  • 16 Shen MC, Lin JS, Tsay W. Protein C and protein S deficiencies are the most important risk factors associated with thrombosis in Chinese venous thrombophilic patients in Taiwan. Thromb Res 2000; 99: 447-452.
    CrossrefPubMedGoogle Scholar
  • 17 Peng YY, Jeng JS, Shen MC. et al. Aetiologies and prognosis of Chinese patients with deep vein thrombosis of the lower extremities. QJM 1998; 91: 681-686.
    CrossrefPubMedGoogle Scholar
  • 18 Kroger K, Weiland D, Ose C. et al. Risk factors for venous thromboembolic events in cancer patients. Ann Oncol 2006; 17: 297-303.
    CrossrefPubMedGoogle Scholar
  • 19 Khorana AA, Kuderer NM, Culakova E. et al. Development and validation of a predictive model for chemotherapy-associated thrombosis. Blood 2008; 111: 4902-4907.
    CrossrefPubMedGoogle Scholar
  • 20 Khorana AA, Connolly GC. Assessing risk of venous thromboembolism in the patient with cancer. J Clin Oncol 2009; 27: 4839-4847.
    CrossrefPubMedGoogle Scholar
  • 21 Connolly GC, Khorana AA. Emerging risk stratification approaches to cancer-associated thrombosis: risk factors, biomarkers and a risk score. Thromb Res 2010; 125 (Suppl. 02) S1-7.
    PubMedGoogle Scholar
  • 22 Lyman GH, Khorana AA, Falanga A. et al. American Society of Clinical Oncology guideline: recommendations for venous thromboembolism prophylaxis and treatment in patients with cancer. J Clin Oncol 2007; 25: 5490-5505.
    CrossrefPubMedGoogle Scholar
  • 23 Khorana AA, Streiff MB, Farge D. et al. Venous thromboembolism prophylaxis and treatment in cancer: a consensus statement of major guidelines panels and call to action. J Clin Oncol 2009; 27: 4919-4926.
    CrossrefPubMedGoogle Scholar
  • 24 Mandala M, Falanga A, Roila F. Venous thromboembolism in cancer patients: ESMO Clinical Practice Guidelines for the management. Ann Oncol 2010; 21 (Suppl. 05) v274-276.
    CrossrefPubMedGoogle Scholar
  • 25 Chen YC, Yeh HY, Wu JC. et al. Taiwan's National Health Insurance Research Database: administrative health care database as study object in bibliometrics. Scientometrics 2010; 86: 365-380.
    PubMedGoogle Scholar
  • 26 Cheng CL, Kao YH, Lin SJ. et al. Validation of the National Health Insurance Research Database with ischemic stroke cases in Taiwan. Pharmacoepidemiol Drug Saf 2011; 20: 236-242.
    CrossrefPubMedGoogle Scholar
  • 27 Tamariz L, Harkins T, Nair V. A systematic review of validated methods for identifying venous thromboembolism using administrative and claims data. Pharmacoepidemiol Drug Saf 2012; 21 (Suppl. 01) 154-162.
    CrossrefPubMedGoogle Scholar
  • 28 Anderson Jr. FA, Wheeler HB, Goldberg RJ. et al. A population-based perspective of the hospital incidence and case-fatality rates of deep vein thrombosis and pulmonary embolism. The Worcester DVT Study. Arch Intern Med 1991; 151: 933-938.
    CrossrefPubMedGoogle Scholar
  • 29 Silverstein MD, Heit JA, Mohr DN. et al. Trends in the incidence of deep vein thrombosis and pulmonary embolism: a 25-year population-based study. Arch Intern Med 1998; 158: 585-593.
    CrossrefPubMedGoogle Scholar
  • 30 Spencer FA, Emery C, Lessard D. et al. The Worcester Venous Thromboembolism study: a population-based study of the clinical epidemiology of venous thromboembolism. J Gen Intern Med 2006; 21: 722-727.
    CrossrefPubMedGoogle Scholar
  • 31 Lee CH, Cheng CL, Chang CH. et al. Universal pharmacological thromboprophylaxis for total knee arthroplasty may not be necessary in low-risk populations: a nationwide study in Taiwan. J Thromb Haemost 2012; 10: 56-63.
    CrossrefPubMedGoogle Scholar
  • 32 Khorana AA, Francis CW, Culakova E. et al. Thromboembolism in hospitalized neutropenic cancer patients. J Clin Oncol 2006; 24: 484-490.
    CrossrefPubMedGoogle Scholar
  • 33 Khorana AA, Francis CW, Culakova E. et al. Frequency, risk factors, and trends for venous thromboembolism among hospitalized cancer patients. Cancer 2007; 110: 2339-2346.
    CrossrefPubMedGoogle Scholar
  • 34 Blom JW, Vanderschoot JP, Oostindier MJ. et al. Incidence of venous thrombosis in a large cohort of 66,329 cancer patients: results of a record linkage study. J Thromb Haemost 2006; 4: 529-535.
    CrossrefPubMedGoogle Scholar
  • 35 Mandala M, Barni S, Floriani I. et al. Incidence and clinical implications of venous thromboembolism in advanced colorectal cancer patients: the 'GISCAD-alternating schedule' study findings. Eur J Cancer 2009; 45: 65-73.
    CrossrefPubMedGoogle Scholar
  • 36 Pritchard KI, Paterson AH, Paul NA. et al. Increased thromboembolic complications with concurrent tamoxifen and chemotherapy in a randomized trial of adjuvant therapy for women with breast cancer. National Cancer Institute of Canada Clinical Trials Group Breast Cancer Site Group. J Clin Oncol 1996; 14: 2731-2737.
    CrossrefPubMedGoogle Scholar
  • 37 Blanco-Molina A, Trujillo-Santos J, Tirado R. et al. Venous thromboembolism in women using hormonal contraceptives. Findings from the RIETE Registry. Thromb Haemost 2009; 101: 478-482.
    Article in Thieme ConnectPubMedGoogle Scholar
  • 38 Potosky AL, Saxman S, Wallace RB. et al. Population variations in the initial treatment of non-small-cell lung cancer. J Clin Oncol 2004; 22: 3261-3268.
    CrossrefPubMedGoogle Scholar
  • 39 Blom JW, Osanto S, Rosendaal FR. High risk of venous thrombosis in patients with pancreatic cancer: a cohort study of 202 patients. Eur J Cancer 2006; 42: 410-414.
    CrossrefPubMedGoogle Scholar
  • 40 Mandala M, Reni M, Cascinu S. et al. Venous thromboembolism predicts poor prognosis in irresectable pancreatic cancer patients. Ann Oncol 2007; 18: 1660-1665.
    CrossrefPubMedGoogle Scholar
  • 41 Menapace LA, Peterson DR, Berry A. et al. Symptomatic and incidental thromboembolism are both associated with mortality in pancreatic cancer. Thromb Haemost 2011; 106: 371-378.
    Article in Thieme ConnectPubMedGoogle Scholar
  • 42 Oh SY, Kim JH, Lee KW. et al. Venous thromboembolism in patients with pancreatic adenocarcinoma: lower incidence in Asian ethnicity. Thromb Res 2008; 122: 485-490.
    CrossrefPubMedGoogle Scholar
  • 43 Lee AY, Levine MN. Venous thromboembolism and cancer: risks and outcomes. Circulation 2003; 107: I17-21.
    PubMedGoogle Scholar
  • 44 Lee KW, Bang SM, Kim S. et al. The incidence, risk factors and prognostic implications of venous thromboembolism in patients with gastric cancer. J Thromb Haemost 2010; 8: 540-547.
    CrossrefPubMedGoogle Scholar