Risk Factors and Prediction Models for Venous Thromboembolism in Ambulatory Patients with Lung Cancer
Abstract
:1. Background and Introduction
2. VTE Risk Factors in Ambulatory Patients with Lung Cancer
3. Risk Prediction Models for VTE in Patients with Cancer
3.1. The Khorana Score
3.2. Modifications of the Khorana Score
3.3. The COMPASS-CAT Score
3.4. Models Developed in Ambulatory Patients with Lung Cancer
4. Risk of Bias in VTE Risk Model Development and Validation Studies
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Fernandes, C.; Morinaga, L.; Alves, J.; Castro, M.; Calderaro, D.; Jardim, C.; Souza, R. Cancer-associated thrombosis: The when, how and why. Eur. Respir. Rev. 2019, 28, 180119. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Timp, J.; Braekkan, S.K.; Versteeg, H.H.; Cannegieter, S.C. Epidemiology of cancer-associated venous thrombosis. Blood 2013, 122. [Google Scholar] [CrossRef] [Green Version]
- Blom, J.W.; Doggen, C.J.; Osanto, S.; Rosendaal, F.R. Malignancies, prothrombotic mutations, and the risk of venous thrombosis. JAMA 2005, 293, 715–722. [Google Scholar] [CrossRef]
- Kenmotsu, H.; Notsu, A.; Mori, K.; Omori, S.; Tsushima, T.; Satake, Y.; Miki, Y.; Abe, M.; Ogiku, M.; Nakamura, T.; et al. Cumulative incidence of venous thromboembolism in patients with advanced cancer in prospective observational study. Cancer Med. 2021, 10, 895–904. [Google Scholar] [CrossRef] [PubMed]
- Connolly, G.C.; Dalal, M.; Lin, J.; Khorana, A.A. Incidence and predictors of venous thromboembolism (VTE) among ambulatory patients with lung cancer. Lung Cancer 2012, 78. [Google Scholar] [CrossRef] [PubMed]
- Chew, H.K.; Davies, A.M.; Wun, T.; Harvey, D.; Zhou, H.; White, R.H. The incidence of venous thromboembolism among patients with primary lung cancer. J. Thromb. Haemost. 2008, 6. [Google Scholar] [CrossRef]
- Streiff, M.; Abutalib, S.A.; Farge, D.; Murphy, M.; Connors, J.M.; Piazza, G. Update on Guidelines for the Management of Cancer-Associated Thrombosis. Oncologist 2021, 26, e24–e40. [Google Scholar] [CrossRef]
- Fuentes, H.; Oramas, D.M.; Paz, L.H.; Casanegra, A.I.; Mansfield, A.S.; Tafur, A.J. Meta-analysis on anticoagulation and prevention of thrombosis and mortality among patients with lung cancer. Thromb. Res. 2017, 154, 28–34. [Google Scholar] [CrossRef]
- Carrier, M.; Abou-Nassar, K.; Mallick, R.; Tagalakis, V.; Shivakumar, S.; Schattner, A.; Kuruvilla, P.; Hill, D.; Spadafora, S.; Marquis, K.; et al. Apixaban to Prevent Venous Thromboembolism in Patients with Cancer. N. Engl. J. Med. 2019, 380, 711–719. [Google Scholar] [CrossRef]
- Key, N.S.; Khorana, A.A.; Kuderer, N.M.; Bohlke, K.; Lee, A.Y.Y.; Arcelus, J.I.; Wong, S.L.; Balaban, E.P.; Flowers, C.R.; Francis, C.W.; et al. Venous Thromboembolism Prophylaxis and Treatment in Patients With Cancer: ASCO Clinical Practice Guideline Update. J. Clin. Oncol. 2020, 38, 496–520. [Google Scholar] [CrossRef]
- Wang, T.F.; Zwicker, J.I.; Ay, C.; Pabinger, I.; Falanga, A.; Antic, D.; Noble, S.; Khorana, A.A.; Carrier, M.; Meyer, G. The use of direct oral anticoagulants for primary thromboprophylaxis in ambulatory cancer patients: Guidance from the SSC of the ISTH. J. Thromb. Haemost. 2019, 17, 1772–1778. [Google Scholar] [CrossRef] [Green Version]
- NCCN. Guidelines for Venous Thromboembolic Disease; Version 1; NCCN: Plymouth Meeting, PA, USA, 2019. [Google Scholar]
- Sabatino, J.; De Rosa, S.; Polimeni, A.; Sorrentino, S.; Indolfi, C. Direct Oral Anticoagulants in Patients With Active Cancer: A Systematic Review and Meta-Analysis. JACC CardioOncol. 2020, 2, 428–440. [Google Scholar] [CrossRef]
- Li, A.; Kuderer, N.M.; Garcia, D.A.; Khorana, A.A.; Wells, P.S.; Carrier, M.; Lyman, G.H. Direct oral anticoagulant for the prevention of thrombosis in ambulatory patients with cancer: A systematic review and meta-analysis. J. Thromb. Haemost. 2019, 17, 2141–2151. [Google Scholar] [CrossRef]
- Roselli, M.; Riondino, S.; Mariotti, S.; La Farina, F.; Ferroni, P.; Guadagni, F. Clinical models and biochemical predictors of VTE in lung cancer. Cancer Metastasis Rev. 2014, 33, 771–789. [Google Scholar] [CrossRef]
- Steyerberg, E.W. Clinical Prediction Models: A Practical Approach to Development, Validation and Updating, 2nd ed.; Springer: Cham, Switzerland, 2019; p. 3. [Google Scholar]
- Khorana, A.; Kuderer, N.M.; Culakova, E.; Lyman, G.H.; Francis, C.W. Development and validation of a predictive model for chemotherapy-associated thrombosis. Blood 2008, 111. [Google Scholar] [CrossRef] [Green Version]
- Mulder, F.I.; Candeloro, M.; Kamphuisen, P.W.; Di Nisio, M.; Bossuyt, P.M.; Guman, N.; Smit, K.; Buller, H.R.; van Es, N. The Khorana score for prediction of venous thromboembolism in cancer patients: A systematic review and meta-analysis. Haematologica 2019, 104. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ay, C.; Dunkler, D.; Marosi, C.; Chiriac, A.; Vormittag, R.; Simanek, R.; Quehenberger, P.; Zielinski, C.; Pabinger, I. Prediction of venous thromboembolism in cancer patients. Blood 2010, 116. [Google Scholar] [CrossRef] [PubMed]
- Verso, M.; Agnelli, G.; Barni, S.; Gasparini, G.; Labianca, R. A modified Khorana risk assessment score for venous thromboembolism in cancer patients receiving chemotherapy: The Protecht score. Intern. Emerg. Med. 2012, 7. [Google Scholar] [CrossRef] [PubMed]
- Pelzer, U.; Sinn, M.; Stieler, J.; Riess, H. Primary pharmacological prevention of thromboembolic events in ambulatory patients with advanced pancreatic cancer treated with chemotherapy. Dtsch. Med. Wochenschr. 2013, 138. [Google Scholar] [CrossRef]
- Gerotziafas, G.T.; Taher, A.; Abdel-Razeq, H.; AboElnazar, E.; Spyropoulos, A.C.; El Shemmari, S.; Larsen, A.K.; Elalamy, I. A Predictive Score for Thrombosis Associated with Breast, Colorectal, Lung, or Ovarian Cancer: The Prospective COMPASS-Cancer-Associated Thrombosis Study. Oncologist 2017, 22, 1222–1231. [Google Scholar] [CrossRef] [Green Version]
- Rupa-Matysek, J.; Lembicz, M.; Rogowska, E.K.; Gil, L.; Komarnicki, M.; Batura-Gabryel, H. Evaluation of risk factors and assessment models for predicting venous thromboembolism in lung cancer patients. Med. Oncol. 2018, 35, 63. [Google Scholar] [CrossRef] [Green Version]
- Syrigos, K.; Grapsa, D.; Sangare, R.; Evmorfiadis, I.; Larsen, A.K.; Van Dreden, P.; Boura, P.; Charpidou, A.; Kotteas, E.; Sergentanis, T.N.; et al. Prospective Assessment of Clinical Risk Factors and Biomarkers of Hypercoagulability for the Identification of Patients with Lung Adenocarcinoma at Risk for Cancer-Associated Thrombosis: The Observational ROADMAP-CAT Study. Oncologist 2018, 23, 1372–1381. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kuderer, N.M.; Poniewierski, M.S.; Culakova, E.; Lyman, G.H.; Khorana, A.A.; Pabinger, I.; Agnelli, G.; Liebman, H.A.; Vicaut, E.; Meyer, G.; et al. Predictors of Venous Thromboembolism and Early Mortality in Lung Cancer: Results from a Global Prospective Study (CANTARISK). Oncologist 2018, 23, 247–255. [Google Scholar] [CrossRef] [Green Version]
- Li, Z.; Zhang, G.; Zhang, M.; Mei, J.; Weng, H.; Peng, Z. Development and Validation of a Risk Score for Prediction of Venous Thromboembolism in Patients with Lung Cancer. Clin. Appl. Thromb. Hemost. 2020, 26, 1076029620910793. [Google Scholar] [CrossRef] [Green Version]
- Jadaon, M.M. Epidemiology of Prothrombin G20210A Mutation in the Mediterranean Region. Mediterr. J. Hematol. Infect. Dis. 2011, 3, e2011054. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- De Stefano, V.; Chiusolo, P.; Paciaroni, K.; Leone, G. Epidemiology of factor V Leiden: Clinical implications. Semin. Thromb. Hemost. 1998, 24, 367–379. [Google Scholar] [CrossRef] [PubMed]
- Liu, Y.; Wang, W.; Wu, F.; Gao, G.; Xu, J.; Li, X.; Zhao, C.; Yang, S.; Mao, S.; Pan, Y.; et al. High discrepancy in thrombotic events in non-small cell lung cancer patients with different genomic alterations. Transl. Lung Cancer Res. 2021, 10, 1512–1524. [Google Scholar] [CrossRef]
- Alexander, M.; Burbury, K. A systematic review of biomarkers for the prediction of thromboembolism in lung cancer—Results, practical issues and proposed strategies for future risk prediction models. Thromb. Res. 2016, 148, 63–69. [Google Scholar] [CrossRef]
- Al-Samkari, H.; Leiva, O.; Dagogo-Jack, I.; Shaw, A.; Lennerz, J.; Iafrate, A.J.; Bendapudi, P.K.; Connors, J.M. Impact of ALK Rearrangement on Venous and Arterial Thrombotic Risk in NSCLC. J. Thorac. Oncol. 2020, 15, 1497–1506. [Google Scholar] [CrossRef]
- Dou, F.; Zhang, Y.; Yi, J.; Zhu, M.; Zhang, S.; Zhang, D.; Zhang, Y. Association of ALK rearrangement and risk of venous thromboembolism in patients with non-small cell lung cancer: A prospective cohort study. Thromb. Res. 2020, 186, 36–41. [Google Scholar] [CrossRef]
- Zer, A.; Moskovitz, M.; Hwang, D.M.; Hershko-Klement, A.; Fridel, L.; Korpanty, G.J.; Dudnik, E.; Peled, N.; Shochat, T.; Leighl, N.B.; et al. ALK-Rearranged Non-Small-Cell Lung Cancer Is Associated With a High Rate of Venous Thromboembolism. Clin. Lung Cancer 2017, 18, 156–161. [Google Scholar] [CrossRef]
- Yang, S.; Yang, L.; Wu, Y.; Zhang, C.; Wang, S.; Ma, N.; Wang, L.; Wang, Q. Anaplastic lymphoma kinase rearrangement may increase the incidence of venous thromboembolism by increasing tissue factor expression in advanced lung adenocarcinoma. Ann. Transl. Med. 2020, 8, 1307. [Google Scholar] [CrossRef] [PubMed]
- Alexander, M.; Solomon, B.; Burbury, K. Thromboembolism in Anaplastic Lymphoma Kinase-Rearranged Non-Small Cell Lung Cancer. Clin. Lung Cancer 2018, 19, e71–e72. [Google Scholar] [CrossRef]
- Hohl Moinat, C.; Périard, D.; Grueber, A.; Hayoz, D.; Magnin, J.-L.; André, P.; Kung, M.; Betticher, D.C. Predictors of venous thromboembolic events associated with central venous port insertion in cancer patients. J. Oncol. 2014, 2014, 743181. [Google Scholar] [CrossRef] [PubMed]
- Moik, F.; Chan, W.E.; Wiedemann, S.; Hoeller, C.; Tuchmann, F.; Aretin, M.B.; Fuereder, T.; Zöchbauer-Müller, S.; Preusser, M.; Pabinger, I.; et al. Incidence, risk factors, and outcomes of venous and arterial thromboembolism in immune checkpoint inhibitor therapy. Blood 2021, 137, 1669–1678. [Google Scholar] [CrossRef]
- Sato, R.; Imamura, K.; Sakata, S.; Ikeda, T.; Horio, Y.; Iyama, S.; Akaike, K.; Hamada, S.; Jodai, T.; Nakashima, K.; et al. Disorder of Coagulation-Fibrinolysis System: An Emerging Toxicity of Anti-PD-1/PD-L1 Monoclonal Antibodies. J. Clin. Med. 2019, 8, 762. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Swaidani, S.; Roopkumar, J.; Jun-Shim, Y.; Charles, C.; Paul, S.; Kundu, S.; Funchain, P.; Rayman, P.; Pavicic, P.G.; Diaz-Montero, C.; et al. Biomarker Assessment of Venous Thromboembolism in Cancer Patients Receiving Checkpoint Blockade. Blood 2019, 134 (Suppl. 1). [Google Scholar] [CrossRef]
- Hoffbrand, A.; Moss, P.A.H. Thrombosis 1: Pathogenesis and Diagnosis. In Hoffbrand’s Essential Haematology, 7th ed.; John Wiley & Sons: Chichester, UK, 2016; Charpter 27. [Google Scholar]
- Koupenova, M.; Clancy, L.; Corkrey, H.A.; Freedman, J.E. Circulating Platelets as Mediators of Immunity, Inflammation, and Thrombosis. Circ. Res. 2018, 122, 337–351. [Google Scholar] [CrossRef]
- Ma, R.; Bi, Y.; Kou, J.; Zhou, J.; Shi, J. Enhanced procoagulant activity of platelets after chemotherapy in non-small cell lung cancer. Cancer Biol. Ther. 2017, 18, 627–634. [Google Scholar] [CrossRef] [Green Version]
- Rangarajan, S. Von Willebrand factor—Two sides and the edge of a coin. Haemophilia 2011, 17, 61–64. [Google Scholar] [CrossRef]
- Pépin, M.; Kleinjan, A.; Hajage, D.; Büller, H.R.; Di Nisio, M.; Kamphuisen, P.W.; Salomon, L.; Veyradier, A.; Stepanian, A.; Mahé, I. ADAMTS-13 and von Willebrand factor predict venous thromboembolism in patients with cancer. J. Thromb. Haemost. 2016, 14, 306–315. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Obermeier, H.L.; Riedl, J.; Ay, C.; Koder, S.; Quehenberger, P.; Bartsch, R.; Kaider, A.; Zielinski, C.C.; Pabinger, I. The role of ADAMTS-13 and von Willebrand factor in cancer patients: Results from the Vienna Cancer and Thrombosis Study. Res. Pract. Thromb. Haemost. 2019, 3, 503–514. [Google Scholar] [CrossRef] [Green Version]
- Lundbech, M.; Krag, A.E.; Christensen, T.D.; Hvas, A.M. Thrombin generation, thrombin-antithrombin complex, and prothrombin fragment F1+2 as biomarkers for hypercoagulability in cancer patients. Thromb. Res. 2020, 186, 80–85. [Google Scholar] [CrossRef]
- Gabazza, E.; Taguchi, O.; Yamakami, T.; Machishi, M.; Ibata, H.; Suzuki, S. Evaluating prethrombotic state in lung cancer using molecular markers. Chest 1993, 103, 196–200. [Google Scholar] [CrossRef]
- Xiong, W.; Zhao, Y.; Xiong, Y.; Xu, M.; Pudasaini, B.; Du, H.; Guo, X. Coagulation factor IV is an indicator of symptomatic pulmonary embolism in patients with primary lung cancer. Clin. Respir. J. 2020, 14, 124–131. [Google Scholar] [CrossRef] [PubMed]
- Iiu, Y.; Gu, Y.; Yi, F.; Cao, B. Retrospective Analysis of Risk Factors for Venous Thromboembolism in 283 Patients with Lung Cancer during Systemic Therapy. Chin. J. Lung Cancer 2019, 22, 419–426. [Google Scholar] [CrossRef]
- Kadlec, B.; Skrickova, J.; Merta, Z.; Dusek, L.; Jarkovsky, J. The incidence and predictors of thromboembolic events in patients with lung cancer. Sci. World J. 2014, 2014, 125706. [Google Scholar] [CrossRef]
- Alexander, M.; Ball, D.; Solomon, B.; MacManus, M.; Manser, R.; Riedel, B.; Westerman, D.; Evans, S.M.; Wolfe, R.; Burbury, K. Dynamic Thromboembolic Risk Modelling to Target Appropriate Preventative Strategies for Patients with Non-Small Cell Lung Cancer. Cancers 2019, 11, 50. [Google Scholar] [CrossRef] [Green Version]
- Falanga, A.; Russo, L.; Milesi, V.; Vignoli, A. Mechanisms and risk factors of thrombosis in cancer. Crit. Rev. Oncol. Hematol. 2017, 118, 79–83. [Google Scholar] [CrossRef] [PubMed]
- Faria, A.; Andrade, S.S.; Peppelenbosch, M.P.; Ferreira-Halder, C.V.; Fuhler, G.M. Platelets in aging and cancer—“Double-edged sword”. Cancer Metastasis Rev. 2020, 39, 1205–1221. [Google Scholar] [CrossRef]
- Gabazza, E.; Taguchi, O.; Yamakami, T.; Machishi, M.; Ibata, H.; Suzuki, S. Correlation between increased granulocyte elastase release and activation of blood coagulation in patients with lung cancer. Cancer 1993, 72, 2134–2140. [Google Scholar] [CrossRef]
- Cowley, L.E.; Farewell, D.M.; Maguire, S.; Kemp, A.M. Methodological standards for the development and evaluation of clinical prediction rules: A review of the literature. Diagn. Progn. Res. 2019, 3, 16. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Vathiotis, I.; Dimakakos, E.P.; Boura, P.; Ntineri, A.; Charpidou, A.; Gerotziafas, G.; Syrigos, K. Khorana Score: Νew Predictor of Early Mortality in Patients with Lung Adenocarcinoma. Clin. Appl. Thromb. Hemost. 2018, 24, 1347–1351. [Google Scholar] [CrossRef]
- Mansfield, A.S.; Tafur, A.J.; Wang, C.E.; Kourelis, T.V.; Wysokinska, E.M.; Yang, P. Predictors of active cancer thromboembolic outcomes: Validation of the Khorana score among patients with lung cancer. J. Thromb. Haemost. 2016, 14, 1773–1778. [Google Scholar] [CrossRef] [Green Version]
- Van Es, N.; Ventresca, M.; Di Nisio, M.; Zhou, Q.; Noble, S.; Crowther, M.; Briel, M.; Garcia, D.; Lyman, G.H.; Macbeth, F.; et al. The Khorana score for prediction of venous thromboembolism in cancer patients: An individual patient data meta-analysis. J. Thromb. Haemost. 2020, 18, 1940–1951. [Google Scholar] [CrossRef]
- Ferroni, P.; Martini, F.; Portarena, I.; Massimiani, G.; Riondino, S.; La Farina, F.; Mariotti, S.; Guadagni, F.; Roselli, M. Novel high-sensitive D-dimer determination predicts chemotherapy-associated venous thromboembolism in intermediate risk lung cancer patients. Clin. Lung Cancer 2012, 13, 482–487. [Google Scholar] [CrossRef]
- Spyropoulos, A.; Eldredge, J.B.; Anand, L.N.; Zhang, M.Q.; Michael, N.; Soheila, R.; David, J. External Validation of a Venous Thromboembolic Risk Score for Cancer Outpatients with Solid Tumors: The COMPASS-CAT Venous Thromboembolism Risk Assessment Model. Oncologist 2020, 25, e1083–e1090. [Google Scholar] [CrossRef] [Green Version]
- Khorana, A.A.; Soff, G.A.; Kakkar, A.K.; Vadhan-Raj, S.; Riess, H.; Wun, T.; Streiff, M.B.; Garcia, D.A.; Liebman, H.A.; Belani, C.P.; et al. Rivaroxaban for Thromboprophylaxis in High-Risk Ambulatory Patients with Cancer. N. Engl. J. Med. 2019, 380, 720–728. [Google Scholar] [CrossRef]
- Rojas-Hernandez, C.; Tang, V.K.; Sanchez-Petitto, G.; Qiao, W.; Richardson, M.; Escalante, C. Development of a clinical prediction tool for cancer-associated venous thromboembolism (CAT): The MD Anderson Cancer Center CAT model. Support. Care Cancer 2020, 28, 3755–3761. [Google Scholar] [CrossRef]
- Pabinger, I.; van Es, N.; Heinze, G.; Posch, F.; Riedl, J.; Reitter, E.M.; Di Nisio, M.; Cesarman-Maus, G.; Kraaijpoel, N.; Zielinski, C.C.; et al. A clinical prediction model for cancer-associated venous thromboembolism: A development and validation study in two independent prospective cohorts. Lancet Haematol. 2018, 5, e289–e298. [Google Scholar] [CrossRef]
- Wolff, R.F.; Moons, K.G.M.; Riley, R.D.; Whiting, P.F.; Westwood, M.; Collins, G.S.; Reitsma, J.B.; Kleijnen, J.; Mallett, S.; PROBAST Group. PROBAST: A Tool to Assess the Risk of Bias and Applicability of Prediction Model Studies. Ann. Intern. Med. 2019, 170, 51–58. [Google Scholar] [CrossRef] [Green Version]
- Moons, K.G.M.; Wolff, R.F.; Riley, R.D.; Whiting, P.F.; Westwood, M.; Collins, G.S.; Reitsma, J.B.; Kleijnen, J.; Mallett, S. PROBAST: A Tool to Assess Risk of Bias and Applicability of Prediction Model Studies: Explanation and Elaboration. Ann. Intern. Med. 2019, 170, W1–W33. [Google Scholar] [CrossRef] [Green Version]
- Van Calster, B.; McLernon, D.J.; van Smeden, M.; Wynants, L.; Steyerberg, E.W.; On behalf of Topic Group ‘Evaluating diagnostic, tests prediction models’ of the Stratos initiative. Calibration: The Achilles heel of predictive analytics. BMC Med. 2019, 17, 230. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wolbers, M.; Koller, M.T.; Witteman, J.C.; Steyerberg, E.W. Prognostic models with competing risks: Methods and application to coronary risk prediction. Epidemiology 2009, 20, 555–561. [Google Scholar] [CrossRef] [PubMed]
- Martins, T.; Annichino-Bizzacchi, J.M.; Romano, A.V.C.; Maciel, F.R. Artificial neural networks for prediction of recurrent venous thromboembolism. Int. J. Med. Inform. 2020, 141, 104221. [Google Scholar] [CrossRef] [PubMed]
- Gerotziafas, G.; Mahé, I.; Lefkou, E.; AboElnazar, E.; Abdel-Razeq, H.; Taher, A.; Antic, D.; Elalamy, I.; Syrigos, K.; Van Dreden, P. Overview of risk assessment models for venous thromboembolism in ambulatory patients with cancer. Thromb. Res. 2020, 191 (Suppl. 1), S50–S57. [Google Scholar] [CrossRef]
Name of Model (Author, Year) | Cancer Type for Model Derivation | Predictors | Score | High Risk | Validated By First Author, Year | Cancer Type for Model Validation |
---|---|---|---|---|---|---|
Khorana Score (Khorana, 2008) [17] | various | Cancer tissue: | Score ≥ 3 # | Alexander 2019 [51] | NSCLC | |
| 2 | |||||
| 1 | van Es 2020 [58] | Various (lung cancer 58%) | |||
Platelet count ≥ 350 × 109/L | 1 | Vathiotis 2018 [56] | Lung adenocarcinoma | |||
Haemoglobin < 100 g/L and/or use of ESA | 1 | Kuderer 2018 [25] | Lung cancer (84% NSCLC) | |||
Leukocyte count >11 × 109/L | 1 | Rupa-Matysek 2018 [23] | Lung cancer (97/118 NSCLC) | |||
BMI ≥ 35 kg/m2 | 1 | Mansfield 2016 [57] | Lung cancer (87.1% NSCLC) | |||
PROTECHT (Verso 2012) [20] | various | As Khorana Score, but | Score ≥ 3 | Alexander 2019 [51] | NSCLC | |
adds gemcitabine chemotherapy, and | 1 | Rupa-Matysek 2018 [23] | Lung cancer (NSCLC 97/118) | |||
platinum chemotherapy | 1 | |||||
CONKO (Pelzer 2013) [21] | various | As Khorana Score, but s | Score ≥ 3 | Alexander 2019 [51] | NSCLC | |
removes BMI ≥ 35 kg/m2, and | Rupa-Matysek 2018 [23] | Lung cancer (NSCLC 97/118) | ||||
adds ECOG PS ≥ 2 | 1 | |||||
COMPASS-CAT (Gerotziafas 2017) [22] | Various (13% lung cancer) | Anthracycline treatment | 6 | Score ≥ 7 | Spyropoulos 2020 [60] | Various (29.05% lung cancer) |
Time since cancer diagnosis ≤ 6 months | 4 | |||||
Central venous catheter | 3 | |||||
Advanced stage of cancer | 2 | |||||
Cardiovascular risk factors present | 5 | Syrigos 2018 [24] | Lung adenocarcinoma | |||
Hospitalisation for acute medical Illness | 2 | Score ≥ 11 | Rupa-Matysek 2018 [23] | Lung cancer (97/118 NSCLC) | ||
A history of VTE | 1 | |||||
Platelet count ≥ 350 × 109/L | 2 | |||||
ROADMAP-CAT (Syrigos 2018) [24] | Lung adenocarcinoma | Procoag-PPL < 44 s, and MRI < 125 nM/min | 1 † | score = 1 | ||
HS D-dimer (Ferroni 2012) [59] | Lung cancer | Khorana Score intermediate group adds high-sensitive D-Dimer | Khorana Score 1–2 and HS D-dimer ≥ 1500 ng/mL | |||
Model 1 (Alexander 2019) [51] | NSCLC | Baseline fibrinogen ≥ 4.0 g/L and baselie D-dimer ≥ 0.5 mg/L | 1 | Score ≥ 1 | Underway ACTRN12618000811202 [51] | NSCLC |
Baseline D-dimer ≥ 1.5 mg/L | 1 | |||||
Month-1 D-dimer ≥ 1.5 mg/L | 1 |
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Yan, A.-R.; Samarawickrema, I.; Naunton, M.; Peterson, G.M.; Yip, D.; De Rosa, S.; Mortazavi, R. Risk Factors and Prediction Models for Venous Thromboembolism in Ambulatory Patients with Lung Cancer. Healthcare 2021, 9, 778. https://doi.org/10.3390/healthcare9060778
Yan A-R, Samarawickrema I, Naunton M, Peterson GM, Yip D, De Rosa S, Mortazavi R. Risk Factors and Prediction Models for Venous Thromboembolism in Ambulatory Patients with Lung Cancer. Healthcare. 2021; 9(6):778. https://doi.org/10.3390/healthcare9060778
Chicago/Turabian StyleYan, Ann-Rong, Indira Samarawickrema, Mark Naunton, Gregory M. Peterson, Desmond Yip, Salvatore De Rosa, and Reza Mortazavi. 2021. "Risk Factors and Prediction Models for Venous Thromboembolism in Ambulatory Patients with Lung Cancer" Healthcare 9, no. 6: 778. https://doi.org/10.3390/healthcare9060778