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Cancer-associated thrombosis: the when, how and why

Caio J. Fernandes, Luciana T. K. Morinaga, José L. Alves  Jr, Marcela A. Castro, Daniela Calderaro, Carlos V. P. Jardim, Rogerio Souza
European Respiratory Review 2019 28: 180119; DOI: 10.1183/16000617.0119-2018
Caio J. Fernandes
Dept of Cardiopulmonology, Heart Institute, University of Sao Paulo Medical School, Sao Paulo, Brazil
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  • ORCID record for Caio J. Fernandes
  • For correspondence: cjcfernandes@yahoo.com.br
Luciana T. K. Morinaga
Dept of Cardiopulmonology, Heart Institute, University of Sao Paulo Medical School, Sao Paulo, Brazil
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José L. Alves  Jr
Dept of Cardiopulmonology, Heart Institute, University of Sao Paulo Medical School, Sao Paulo, Brazil
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Marcela A. Castro
Dept of Cardiopulmonology, Heart Institute, University of Sao Paulo Medical School, Sao Paulo, Brazil
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Daniela Calderaro
Dept of Cardiopulmonology, Heart Institute, University of Sao Paulo Medical School, Sao Paulo, Brazil
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Carlos V. P. Jardim
Dept of Cardiopulmonology, Heart Institute, University of Sao Paulo Medical School, Sao Paulo, Brazil
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Rogerio Souza
Dept of Cardiopulmonology, Heart Institute, University of Sao Paulo Medical School, Sao Paulo, Brazil
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Tables

  • TABLE 1

    Relative risk of venous thromboembolism diagnosis in hospitalised cancer patients

    CancersOdds ratio
    Haematological cancer26.2
    Lung24.8
    Gastrointestinal (bowel, pancreas, stomach, oesophagus)18.9
    Brain8.0
    Kidney5.8
    Skin (melanoma, squamous cell)3.6
    Breast3.5
    Prostate3.4
    Uterine cervix3.3
    Ovarium2.3
    Ear, nose and throat1.5
    Other6.6

    Data from [19].

    • TABLE 2

      Risk factors for cancer-associated thrombosis

      Patient-related factors
      •  Advanced age

      •  Female sex

      •  Prior venous thromboembolism

      •  Patient comorbidities

      •  Infection, obesity, anaemia, pulmonary or renal disease

      •  Prolonged immobilisation

       Inherited thrombophilic factors
      Cancer-related factors
      •  Site: haematological malignancies, lung, pancreas, stomach, brain, kidney

      •  Stage: advanced stage and initial period after diagnosis

      •  Hospitalisation

      •  Surgery

      •  Chemotherapy and hormonal therapy

      •  Anti-angiogenic therapy

      •  Erythropoiesis-stimulating agents

      •  Blood transfusions

      Candidate biomarkers
      •  Platelet count (>35 0000 per µL)

      •  Leukocyte count (>11 000 per µL)

      •  D-dimer

      •  Tissue factor expression by tumour cells

      •  Circulating tissue factor

      •  Soluble P-selectin

      •  C-reactive protein

      Reproduced from [22] with permission from the publisher.

      • TABLE 3

        Predictive model for chemotherapy-associated venous thromboembolism

        Patient characteristicsRisk score
        Site of cancer
         Very high risk (stomach, pancreas)2
         High risk (lung, lymphoma, gynaecologic, bladder, testicular)1
        Prechemotherapy platelet count ≥350 000 per mm31
        Haemoglobin level <10 g·dL−1 or use of red cell growth factors1
        Prechemotherapy leukocyte count >11 000 per mm31
        Body mass index ≥35 kg·m−21

        A risk score ≥3 is a high-risk score, 1–2 is an intermediate score, and 0 is a low-risk score.

        • TABLE 4

          Major randomised trials in cancer-associated thrombosis primary prophylaxis

          TrialYearPatients nDrugs evaluatedMajor findings
          ENOXACAN II [32]2002332 (submitted for abdominal or pelvic surgery)Enoxaparin (31 days) versus placebo (after 10 days of surgery)Enoxaparin patients presented less VTE events than placebo after 1 (p=0.02) and 3 months (p=0.01). No difference in major bleeding.
          PROTECHT [27]20091150Nadroparin (4 months) versus placeboNadroparin patients presented less thrombotic events (venous and arterial) than placebo (p=0.02). No statistical difference in major bleeding.
          SAVE-ONCO [28]20123212Semuloparin (3.5 months) versus placeboSemuloparin patients presented less VTE events than placebo (p<0.001). No difference in major bleeding.
          AVERT [30]2018563Apixaban (180 days) versus placeboApixaban patients presented less VTE events than placebo (p<0.001) and more major bleeding (p=0.046) than placebo.
          CASSINI [31]2018841Rivaroxaban (180 days) versus placeboStatistical trend of less VTE events and VTE-related death in rivaroxaban patients (p=0.10). No difference in major bleeding.

          VTE: venous thromboembolism.

          • TABLE 5

            Major randomised trials in cancer-associated thrombosis treatment

            TrialYearPatients nDrugs evaluatedMajor findings
            CANTHANOX [35]2002146Enoxaparin versus warfarinStatistical tendency of warfarin to be more associated with major bleeding (p=0.09) and death (p=0.07) than enoxaparin.
            CLOT [36]2003672Dalteparin versus warfarinDalteparin was superior to warfarin in VTE recurrence (p=0.002). No difference in major bleeding or mortality.
            CATCH [37]2015900Tinzaparin versus warfarinStatistical tendency of VTE recurrence reduction with tinzaparin (p=07). No difference in major bleeding or mortality.
            HOKUSAI-CANCER [45]20181046Edoxaban versus dalteparinEdoxaban was non-inferior to dalteparin. Statistical tendency of superiority of edoxaban in VTE recurrence reduction (p=0.09), statistically significant more major bleeding with edoxaban (p=0.04).
            SELECT-D [47]2018406Rivaroxaban versus dalteparinStatistically significant less VTE recurrence (HR 0.43, 95% CI 0.19–0.99) and statistical tendency of more bleeding (HR 1.83, 95% CI 0.68–4.96) with rivaroxaban (oesophagus and gastro-oesophageal junction cancer patients excluded after inclusion of the first 220 patients)
            CARAVAGGIO [48]2019 (expected)1168 (expected)Apixaban versus dalteparin?

            VTE: venous thromboembolism.

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            Cancer-associated thrombosis: the when, how and why
            Caio J. Fernandes, Luciana T. K. Morinaga, José L. Alves, Marcela A. Castro, Daniela Calderaro, Carlos V. P. Jardim, Rogerio Souza
            European Respiratory Review Mar 2019, 28 (151) 180119; DOI: 10.1183/16000617.0119-2018

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            Cancer-associated thrombosis: the when, how and why
            Caio J. Fernandes, Luciana T. K. Morinaga, José L. Alves, Marcela A. Castro, Daniela Calderaro, Carlos V. P. Jardim, Rogerio Souza
            European Respiratory Review Mar 2019, 28 (151) 180119; DOI: 10.1183/16000617.0119-2018
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            • Article
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