Skip to main content
Download PDF

Factors associated with venous thromboembolic disease due to failed thromboprophylaxis

Thrombosis Journal volume 21, Article number: 120 (2023) Cite this article

Abstract

Introduction

Available evidence to identify factors independently associated with failed thromboprophylaxis (FT) in medical patients is insufficient. The present study seeks to evaluate in hospitalized patients, which clinical factors are associated with the development of FT.

Materials and methods

A case-control study nested to a historical cohort, comparing patients who developed failed thromboprophylaxis (cases) with those who did not (controls). Univariate and multivariate regression analysis was performed to define the factors associated with FT.

Results

We selected 204 cases and 408 controls (52.4% men, median age 63 years). Medical patients were 78.4%. The most frequent thromboprophylaxis scheme was enoxaparin. In the failed thromboprophylaxis group, most of the embolic events corresponded to pulmonary embolism (53.4%). Among cases, BMI was higher (26.3 vs. 25 kg/m2, p < 0.001), as was the proportion of patients with leukocytosis > 13,000 (27% vs. 18.9%, p:0.22), and patients who required intensive care management (48% vs. 24.8%, p < 0.001). Factors independently associated with FT were BMI (OR1.04;95%CI 1.00-1.09, p:0.39), active cancer (OR:1.63;95%IC 1.03–2.57, p:0.04), leukocytosis (OR:1.64;95%CI 1.05–2.57, p:0.03) and ICU requirement (OR:3.67;95%CI 2.31–5.83, p < 0.001).

Conclusion

Our study suggests that the failed thromboprophylaxis is associated with high BMI, active cancer, leukocytosis, and ICU requirement. Future studies should evaluate whether there is benefit in adjusting the thromboprophylaxis scheme in patients with one or more of these factors.

Introduction

Venous thromboembolic disease (VTD), defined as pulmonary embolism (PE) and deep vein thrombosis (DVT), is the third most common thromboembolic disease worldwide after acute myocardial infarction and stroke [1]. In the European Union, it causes more than 300,000 deaths [2] and is associated with an estimated cost of up to 8.5 billion euros [3]. It also generates high rates of disability in the short (27.1%) and medium term (7.1%) [4].

Risk factors for developing VTD include hospitalization [5, 6], which is why effective prevention strategies such as pharmacological thromboprophylaxis are used [7, 8]. However, up to 3% of patients on pharmacological thromboprophylaxis may experience thromboembolic events [9], a concept known as failed thromboprophylaxis (FT).

Various strategies have been proposed to reduce the risk of FT in surgical patients, such as increased doses of heparin in patients undergoing bariatric surgery [10, 11], or combined thromboprophylaxis (pharmacological and mechanical with pneumatic compression stockings) in patients at very high surgical risk, as proposed by the American Society of Hematology [12, 13]. At present, there is insufficient evidence to identify the factors independently associated with FT, and this information could help us to develop specific strategies to prevent FT in this population.

The present study investigates which factors are associated with the development of FT in a cohort of predominantly medical inpatients.

Materials and methods

A case-control study, nested in a historical cohort, evaluated patients who received pharmacological thromboprophylaxis at the Hospital Universitario San Ignacio (HUSI) between 1 and 2019 and 31 December 2021, and compared those who presented a venous thromboembolic event despite pharmacological thromboprophylaxis (failed thromboprophylaxis) (cases) with those who did not (controls). Patients over 18 years old, hospitalized for more than 24 h and receiving pharmacological thromboprophylaxis with enoxaparin, unfractionated heparin or dalteparin during their hospital stay, were included. Patients with an indication for full anticoagulation prior to hospital admission were excluded. The study was approved by the institutional research and ethics committee with approval code 206/2021.

Patients were identified using two institutional databases: (1) an electronic registry, in which all patients receiving pharmacological thromboprophylaxis are systematically recorded (were case and controls were present), and (2) an institutional anticoagulation registry, which includes all patients diagnosed with PE and DVT (used to identify cases). Because of the low incidence of failed thromboprophylaxis and the large number of controls, case-control matching was considered on a 1:2 basis, adjusting for age (in ranges +/- 1 year), sex, type of pharmacological thromboprophylaxis, and date of hospitalization (+/- 90 days). When more than one control fulfilled the matching criteria, a randomization was used to select the control finally included in the analysis.

Once patients were identified, the institutional electronic medical records were reviewed for information on height, weight, presence of a central venous catheter, active cancer, history of venous thromboembolism, indication for hospitalization, surgery, missed doses, leukocytosis on admission, blood component transfusion, ICU stay and SARS COV 2 infection. The data were stored using a standardized format.

Cases were defined as patients without clinical suspicion of PE or symptomatic DVT on admission and in whom the diagnosis of acute pulmonary embolism was confirmed during hospitalization by chest angiography, ventilation-perfusion scan and/or confirmation of acute deep vein thrombosis by venous doppler of the lower limbs. Controls were patients with no clinical suspicion of PE or DVT on admission and in whom these were not documented during hospitalization.

Among the variables, pharmacological thromboprophylaxis was defined as treatment with enoxaparin at a dose of 40 mg subcutaneous per day, treatment with unfractionated heparin at a dose of 5000 U subcutaneous every 12 h, or dalteparin at a dose of 5000 U subcutaneous per day. Missed dose was defined as the non-application of pharmacological thromboprophylaxis despite its formulation according to thrombotic risk calculated by the Padua prediction score [14] in medical patients or the Caprini score for venous thromboembolism [15] in surgical patients, either because it was not prescribed by the attending physician or because it was not applied by the nursing staff.

For sample size calculation, we considered evaluating 10 cases for each variable of interest [16]. Considering that we identified 11 variables potentially associated with FT, a minimum required sample size of 110 cases and 220 controls was calculated. Categorical variables were reported as absolute numbers and percentages. Continuous variables were reported as median and interquartile range, as the assumption of normality was not met using the Shappiro-Wilk test. The t-test, Mann-Whitney U test or chi-squared test were used to compare cases and controls, depending on the type of variable. Finally, odds ratios (ORs) were calculated using a conditional logistic regression model with fixed effects, reporting first a univariate analysis and then a multivariate analysis, including in the analysis the variables that were significant in the univariate model or those reported to be associated with FT in previous studies. The selection of variables to be included in the final model was performed using the stepwise backward method. Those with a value of p < 0.05 were considered significant. The statistical package Stata 16 [17] was used for analysis. (Stata Statistical Software: Release 16. College Station, TX: Stata Corp LLC).

Results

There were 1200 patients identified in the iinstitutional anticoagulation registry,, with newly diagnosed PE or DVT. Of this, 204 patients were identified to fulfill criteria for failed thromboprophylaxis (cases), accounting for 17% of all events. Of the 29,104 patients identified in the electronic thromboprophylaxis registry who received thromboprophylaxis and had no events (controls), we selected 408 patients matched by age, type of thromboprophylaxis, sex and time of hospitalization.

Most patients were male, with a median age of 63 years (IQR 51–74). Patients with a non-surgical indication for hospitalization were 78.4%. The most reported pharmacological thromboprophylaxis was enoxaparin (92%). 29% of patients in both groups had some form of active cancer.

The comparison between the case and control groups is shown in Table 1. There was higher incidence of hematologic cancer in the control group (33.88% vs. 16.64%), while prostate cancer was more frequent in the case group (4.13% vs. 15.25%) (p: 0.032). In the failed thromboprophylaxis group, most thrombotic events were PE (53.4%). Cases had a higher BMI (26.3 vs. 25 kg/m2, p < 0.001) and a higher proportion of patients with leukocytosis > 13,000 (27% vs. 18.9%, p:0.22). Cases also had more intensive care unit management (48% vs. 24.8%, p < 0.001) and were more frequently associated with SARS COV 2 infection (47.1% vs. 37.1%, p < 0.001). Longer hospitalization was observed in the case group (Median 19 days, IQR 12–30 vs. 13 days, IQR 7–21, p < 0.01), with a median of time since admission to VTE diagnosis in the case group of 8.5 days (IQR 5–15).

Table 1 Demographic and clinical characteristics of patients with failed and successful thromboprophylaxis
Full size table

Table 2 shows the univariate and multivariate analysis of factors associated with failed thromboprophylaxis. In univariate analysis, FT was associated with BMI (OR 1.05; CI95% 1.01–1.09, p:0.011), presence of leukocytosis (OR 1.68; CI95% 1.23–2.53, p:0.012), ICU stay (OR 3.31; CI95% 2.23–4.90, p < 0.001) and SARS COV2 infection (OR 1.97; CI95% 1.36–2.87, p < 0.001). Multivariate analysis showed that factors independently associated with the development of FT were BMI (OR 1.04; CI95% 1.00-1.09, p: 0.039), presence of active cancer (OR 1.63; CI95% 1.03–2.57, p:0.036), leukocytosis (OR 1.64; CI95% 1.05–2.57, p:0.031) and ICU stay (OR 3.67; CI95% 2.31–5.83, p < 0.001). SARS COV2 infection was not significantly associated with FT on multivariate analysis (OR 1.29; CI95% 0.78–2.13, p: 0.312).

Table 2 Univariate and multivariate analysis of factors associated with failed thromboprophylaxis
Full size table

Discussion

In this study, we evaluated the clinical factors associated with failed thromboprophylaxis and found that BMI, active cancer, leukocytosis and need for intensive care unit were significantly associated with this outcome.

Obesity is known to be a prothrombotic state secondary to chronic inflammation [18] and is an independent factor that increases the risk of developing VTD by up to 6.2-fold [19]. Our results are consistent with those reported in the literature. To reduce the risk of FT in obese patients, strategies such as increasing the dose of low molecular weight heparin (LMWH) have been evaluated with inconsistent results. In a retrospective cohort study of 1335 patients, the incidence of VTD was similar in the high-dose and low-dose groups, with a higher incidence of bleeding complications in the high-dose group [20]. More recently, a meta-analysis of 6266 patients was published showing that the high-dose group had a lower incidence of VTD (OR: 0.47, 95% CI: 0.27–0.82, p:0.007) and a similar incidence of bleeding events (OR: 0.86, 95% CI: 0.69–1.08) compared with the standard-dose group [21]. Another proposed strategy for thromboprophylaxis in obese patients is to monitor anti-Xa levels and titrate the dose according to the results; however, this strategy also showed no benefit over the usual dose [22] and is therefore not currently recommended. At present, the appropriate dose of LMWH to reduce VTD in patients with a BMI > 30 kg/m2 remains controversial and is not currently recommended in international guidelines; however, this recommendation is likely to change in the future as additional evidence becomes available.

Our results are also consistent with the literature on active cancer as a factor associated with FT; it has been described that the malignant tumor expresses procoagulant proteins that, among other mechanisms, directly activate the coagulation cascade or platelets, thus representing a prothrombotic state [23]. In our study, the case group had a higher incidence of prostate cancer, whereas the control group had a higher incidence of hematologic cancer, however, prostate cancer is not typically associated with a higher incidence of thrombosis than other types of cancer [24], so it is unlikely it could change our results. Oncology patients have a 4.1-fold increased risk of thrombosis, rising to 6.5-fold in the setting of active chemotherapy [6], a risk that may increase during hospitalization. Therefore, the American Hematology Association guidelines for the prevention of thrombotic events consider combined thromboprophylaxis for surgery with high thrombotic risk and low bleeding risk [25]. A randomized clinical trial comparing weight-adjusted versus fixed-dose low-molecular-weight heparin in hospitalized patients found no difference in bleeding; however, the cumulative incidence of VTD at day 14 was 5.9% in the weight-adjusted arm (CI90%, 0-20.5%) [26]. The evidence provided by this study is very limited given the small sample size and lack of control for other potential cofounders such as obesity, so further studies are needed to make a recommendation in medical patients.

Leukocytosis was also associated with FT in our study. Leukocytosis can be caused by a variety of factors including neoplasia, drugs, hypersensitivity reactions and infection [27], with infection being the most common cause. Sepsis has been shown to be an independent risk factor for VTD (OR 1.74; 95%CI, 1.59–1.90). Risk factors associated with sepsis include age, diabetes, chronic kidney disease, chronic obstructive pulmonary disease, stroke, malignancy, and antibiotic use [28], most of which are risk factors for thrombosis. Among septic patients, those requiring mechanical ventilation [29] had a higher risk of thromboprophylaxis failure, suggesting that the greater the severity of the infectious process, the greater the risk of thrombosis.

ICU admission is recognized as a risk factor for failed thromboprophylaxis [30], which is consistent with our study. Risk factors have been identified in ICU patients such as mechanical ventilation (OR 1.56; 95% CI 0.23–10.45, p: 0.64), prolonged immobility (OR 2.14; 95% CI 0.11–40.87, p: 0.61) and femoral venous catheter use (OR 2.24, 95% CI 0.41–12.20, p: 0.35) [31]. In septic patients, ARDS has also been associated with an increased risk of thrombosis [32], all of which may be secondary to the prothrombotic state associated with these conditions. Pharmacological thromboprophylaxis in conjunction with mechanical thromboprophylaxis to reduce failed thromboprophylaxis is being studied and results are awaited [33, 34]; however, there are currently no studies to suggest additional interventions.

Strengths of this study include the high proportion of medical patients; however, the recommendations and findings of this study cannot be generalized to obstetric patients. Although this is an uncommon pathology, the required sample size was exceeded, which means greater statistical power. The results obtained are mostly in line with what has been demonstrated in the clinical literature. Limitations are associated with the case-control design in terms of control selection. We selected controls from a large cohort that included all patients who received thromboprophylaxis in our institution and matched them according to pre-defined criteria. However, residual confounding may be present due to unmeasured confounding variables. To overcome these limitations, large prospective cohorts will be required in the future. Additionally, considering the retrospective nature of our research, a causal relationship cannot be established.

Conclusions

Our study suggests that BMI, active cancer, leukocytosis and need for intensive care are significantly and independently associated with thromboprophylaxis failure. The coexistence of these factors may suggest the use of alternative therapies to minimize this risk. Future studies should evaluate the potential benefits of these therapeutic options in medically managed patients.

Data Availability

All of the material is owned by the authors.

References

  1. Wendelboe AM, Raskob GE. Global burden of Thrombosis: epidemiologic aspects. Circ Res. 2016;118(9):1340–7.

    Article  CAS  PubMed  Google Scholar 

  2. Cohen AT, Agnelli G, Anderson FA, Arcelus JI, Bergqvist D, Brecht JG, et al. Venous thromboembolism (VTE) in Europe - the number of VTE events and associated morbidity and mortality. Thromb Haemost. 2007;98(4):756–64.

    CAS  PubMed  Google Scholar 

  3. Barco S, Woersching AL, Spyropoulos AC, Piovella F, Mahan CE. European Union-28: an annualised cost-of-illness model for venous thromboembolism. Thromb Haemost. 2016;115(4):800–8.

    Article  PubMed  Google Scholar 

  4. Jha AK, Larizgoitia I, Audera-Lopez C, Prasopa-Plaizier N, Waters H, Bates DW. The global burden of unsafe medical care: analytic modelling of observational studies. BMJ Quality &amp; Safety. 2013 Oct 1;22(10):809.

  5. Heit JA, Melton LJ, Lohse CM, Petterson TM, Silverstein MD, Mohr DN et al. Incidence of Venous Thromboembolism in Hospitalized Patients vs Community Residents. Mayo Clin Proc. 2001;76(11):1102–10.

  6. Heit JA, Silverstein MD, Mohr DN, Petterson TM, O’Fallon WM, Melton LJ. Risk factors for deep vein Thrombosis and Pulmonary Embolism: a population-based case-control study. Arch Intern Med. 2000;160(6):809–15.

    Article  CAS  PubMed  Google Scholar 

  7. Dentali F, Douketis JD, Gianni M, Lim W, Crowther MA. Meta-analysis: anticoagulant prophylaxis to prevent symptomatic venous thromboembolism in hospitalized medical patients. Ann Intern Med. 2007;146(4):278–88.

    Article  PubMed  Google Scholar 

  8. Geerts WH, Bergqvist D, Pineo GF, Heit JA, Samama CM, Lassen MR, et al. Prevention of venous thromboembolism: American College of Chest Physicians evidence-based clinical practice guidelines (8th edition). Chest. 2008;133(6 SUPPL):381S–453S.

    Article  CAS  PubMed  Google Scholar 

  9. Northup A, Wilcox S. Thromboprophylaxis failure in the Adult Medical Inpatient. Am J Med Sci. 2017;354(2):107–16.

    Article  PubMed  Google Scholar 

  10. Shepherd MF, Rosborough TK, Schwartz ML. Heparin thromboprophylaxis in gastric bypass Surgery. Obes Surg. 2003;13(2):249–53.

    Article  PubMed  Google Scholar 

  11. Ikesaka R, Delluc A, Le Gal G, Carrier M. Efficacy and safety of weight-adjusted heparin prophylaxis for the prevention of acute venous thromboembolism among obese patients undergoing bariatric Surgery: a systematic review and meta-analysis. Thromb Res. 2014;133(4):682–7.

    Article  CAS  PubMed  Google Scholar 

  12. Anderson DR, Morgano GP, Bennett C, Dentali F, Francis CW, Garcia DA, et al. American Society of Hematology 2019 guidelines for management of venous thromboembolism: prevention of venous thromboembolism in surgical hospitalized patients. Blood Adv. 2019;3(23):3898–944.

    Article  PubMed  PubMed Central  Google Scholar 

  13. Schünemann HJ, Cushman M, Burnett AE, Kahn SR, Beyer-Westendorf J, Spencer FA, et al. American Society of Hematology 2018 guidelines for management of venous thromboembolism: prophylaxis for hospitalized and nonhospitalized medical patients. Blood Adv. 2018;2(22):3198–225.

    Article  PubMed  PubMed Central  Google Scholar 

  14. Barbar S, Noventa F, Rossetto V, Ferrari A, Brandolin B, Perlati M, et al. A risk assessment model for the identification of hospitalized medical patients at risk for venous thromboembolism: the Padua Prediction score. J Thromb Haemost. 2010;8(11):2450–7.

    Article  CAS  PubMed  Google Scholar 

  15. Wilson S, Chen X, Cronin MA, Dengler N, Enker P, Krauss ES, et al. Thrombosis prophylaxis in surgical patients using the Caprini risk score. Curr Probl Surg. 2022;59(11):101221.

    Article  PubMed  Google Scholar 

  16. Harrell FE, Lee KL, Mark DB. Tutorial in bioestadistics multivariable prognostic models: issues in developing models, evaluating assumptions and adequacy, and measuring and reducing errors. Stat Med. 1996;15:361–87.

    Article  PubMed  Google Scholar 

  17. Stata Technical Support. Citing Stata software, documentation, and FAQs [Internet]. College Station, TX: StataCorp LLC.; 2019 [cited 2023 Jun 16]. Available from: https://www.stata.com/support/faqs/resources/citing-software-documentation-faqs/.

  18. Blokhin IO, Lentz SR. Mechanisms of Thrombosis in obesity. Curr Opin Hematol. 2013;20(5):437.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Hotoleanu C. Association between obesity and venous thromboembolism. Med Pharm Rep. 2020;93(2):162.

    PubMed  PubMed Central  Google Scholar 

  20. Joy M, Tharp E, Hartman H, Schepcoff S, Cortes J, Sieg A, et al. Safety and Efficacy of High-Dose Unfractionated Heparin for Prevention of venous thromboembolism in overweight and obese patients. Pharmacotherapy: The Journal of Human Pharmacology and Drug Therapy. 2016;36(7):740–8.

    Article  CAS  Google Scholar 

  21. Liu J, Qiao X, Wu M, Wang H, Luo H, Zhang H, et al. Strategies involving low-molecular-weight heparin for the treatment and prevention of venous thromboembolism in patients with obesity: a systematic review and meta-analysis. Front Endocrinol (Lausanne). 2023;14:1084511.

    Article  PubMed  Google Scholar 

  22. Egan G, Ensom MHH. Measuring anti–factor xa activity to monitor low-molecular-weight heparin in obesity: a critical review. Can J Hosp Pharm. 2015;68(1):33.

    PubMed  PubMed Central  Google Scholar 

  23. Khorana AA, Mackman N, Falanga A, Pabinger I, Noble S, Ageno W, et al. Cancer-associated venous thromboembolism. Nat Reviews Disease Primers 2022. 2022;8(1):1.

    Google Scholar 

  24. Khorana AA, Connolly GC. Assessing risk of venous thromboembolism in the patient with cancer. J Clin Oncol. 2009;27(29):4839–47.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Lyman GH, Carrier M, Ay C, Di Nisio M, Hicks LK, Khorana AA, et al. American Society of Hematology 2021 guidelines for management of venous thromboembolism: prevention and treatment in patients with cancer. Blood Adv. 2021;5(4):927–74.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Zwicker JI, Roopkumar J, Puligandla M, Schlechter BL, Sharda AV, Peereboom D, et al. Dose-adjusted enoxaparin thromboprophylaxis in hospitalized cancer patients: a randomized, double-blinded multicenter phase 2 trial. Blood Adv. 2020;4(10):2254–60.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Mank V, Azhar W, Brown K, Leukocytosis. StatPearls. 2023.

  28. Yeh YT, Tsai SE, Chen YC, Yang SF, Yeh HW, Wang BY et al. Deep venous Thrombosis and risk of consequent Sepsis event: a Retrospective Nationwide Population-based Cohort Study. Int J Environ Res Public Health. 2021;18(15).

  29. Kaplan D, Charles Casper T, Gregory Elliott C, Men S, Pendleton RC, Kraiss LW, et al. VTE incidence and risk factors in patients with severe Sepsis and septic shock. Chest. 2015;148(5):1224–30.

    Article  PubMed  PubMed Central  Google Scholar 

  30. Lim W, Meade M, Lauzier F, Zarychanski R, Mehta S, Lamontagne F, et al. Failure of anticoagulant thromboprophylaxis: risk factors in medical-surgical critically Ill patients. Crit Care Med. 2015;43(2):401–10.

    Article  CAS  PubMed  Google Scholar 

  31. Cook D, Attia J, Weaver B, McDonald E, Meade M, Crowther M. Venous thromboembolic Disease: an observational study in medical-surgical intensive care unit patients. J Crit Care. 2000;15(4):127–32.

    Article  CAS  PubMed  Google Scholar 

  32. Hanify JM, Dupree LH, Johnson DW, Ferreira JA. Failure of chemical thromboprophylaxis in critically ill medical and surgical patients with sepsis. J Crit Care. 2017;37:206–10.

    Article  PubMed  Google Scholar 

  33. Efficacy of the Association Mechanical Prophylaxis + Anticoagulant. Prophylaxis on Venous Thromboembolism Incidence in Intensive Care Unit (ICU) - Full Text View - ClinicalTrials.gov.

  34. Arabi Y, Al-Hameed F, Burns KEA, Mehta S, Alsolamy S, Almaani M et al. Statistical analysis plan for the pneumatic CompREssion for PreVENting venous thromboembolism (PREVENT) trial: a study protocol for a randomized controlled trial. Trials. 2018;19(1).

Download references

Funding

No funding was received.

Author information

Authors and Affiliations

  1. Internal Medicine Department, Faculty of Medicine, Pontificia Universidad Javeriana, Bogotá, Colombia

    Santiago Grillo Pérez, Paula Ruiz-Talero & Oscar Mauricio Muñoz Velandia

  2. Internal Medicine Department, Hospital Universitario San Ignacio, Bogotá, Colombia

    Santiago Grillo Pérez, Paula Ruiz-Talero & Oscar Mauricio Muñoz Velandia

Authors
  1. Santiago Grillo Pérez
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Paula Ruiz-Talero
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Oscar Mauricio Muñoz Velandia
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

All Authors wrote the main manuscript text, prepared tables and reviewed the manuscript.

Corresponding author

Correspondence to Santiago Grillo Pérez.

Ethics declarations

Ethical approval

The present study is subject to the ethical norms of Helsinki and to the Scientific, Technical and Administrative Norms for Health Research Resolution No. 008430 of 1993. According to the same resolution, it is considered research without risk. The confidentiality and reserve of the data obtained was maintained through secure databases.

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Pérez, S.G., Ruiz-Talero, P. & Velandia, O.M.M. Factors associated with venous thromboembolic disease due to failed thromboprophylaxis. Thrombosis J 21, 120 (2023). https://doi.org/10.1186/s12959-023-00566-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1186/s12959-023-00566-4

Keywords

Thrombosis Journal

ISSN: 1477-9560

Contact us