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Cancers
Special Issues
Treatment of Cancer-Associated Thrombosis
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Treatment of Cancer-Associated Thrombosis

A special issue of Cancers (ISSN 2072-6694).

Deadline for manuscript submissions: closed (30 June 2020) | Viewed by 30526

Special Issue Editors

Dr. Corinne Frere

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Guest Editor
INSERM UMRS-1166, Institute of Cardiometabolism and Nutrition, GRC 27 GRECO, Sorbonne Université, F-75013 Paris, France
Interests: hemostasis; thrombosis; cancer-associated thrombosis; intensive care medicine; biomarkers; translational studies
Special Issues, Collections and Topics in MDPI journals
Prof. Dr. Dominique Farge

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Guest Editor
1. Internal Medicine Unit (UF 04): CRMR MATHEC, Maladies Auto-Immunes et Thérapie Cellulaire, Saint-Louis Hospital, Assistance Publique-Hôpitaux de Paris, F-75010 Paris, France
2. Institut Universitaire d’Hématologie, Université de Paris, EA 3518, F-75010 Paris, France
Interests: venous thromboembolism; cancer; decision support systems; clinical practice guidelines; predictive medicine
Special Issues, Collections and Topics in MDPI journals
Dr. Jean M. Connors

E-Mail Website
Guest Editor
Hematology Division, Brigham and Women’s Hospital, Harvard Medical School, Boston, MA 02215, USA
Interests: venous thromboembolism; cancer; decision support systems; clinical practice guidelines; predictive medicine
Special Issues, Collections and Topics in MDPI journals

Special Issue Information

Dear Colleagues,  

Venous thromboembolism (VTE) is a common and life-threatening complication in cancer patients. Cancer patients often suffer from multiple co‐morbidities and have both a greater risk of VTE recurrence and bleeding compared to noncancer patients. For many years, long-term therapy with low-molecular-weight heparin (LMWH) has been the standard of care for the management of cancer-associated thrombosis (CAT), but recent randomized controlled trials have indicated that direct oral anticoagulants (DOAC) are also effective. With the emergence of DOAC as a new option in the treatment of CAT, clinicians are now facing a multitude of choices for each individual patient. A personalized approach, matching the right drug to the right patient based on drug properties, efficacy and safety, the side effect profile of each drug, and patient preference will thus probably supplant the one size fits all approach in the future. This Special Issue will cover the current clinical evidence supporting the standard of care and emerging treatment options for CAT. Data on adherence to CAT clinical practice guidelines and evidence on anticoagulant effects on the quality-of-life perception in cancer patients will be also welcomed.

Dr. Corinne Frere
Prof. Dominique Farge
Dr. Jean M. Connors
Guest Editors

Manuscript Submission Information

Manuscripts should be submitted online at www.mdpi.com by registering and logging in to this website. Once you are registered, click here to go to the submission form. Manuscripts can be submitted until the deadline. All submissions that pass pre-check are peer-reviewed. Accepted papers will be published continuously in the journal (as soon as accepted) and will be listed together on the special issue website. Research articles, review articles as well as communications are invited. For planned papers, a title and short abstract (about 100 words) can be sent to the Editorial Office for announcement on this website.

Submitted manuscripts should not have been published previously, nor be under consideration for publication elsewhere (except conference proceedings papers). All manuscripts are thoroughly refereed through a single-blind peer-review process. A guide for authors and other relevant information for submission of manuscripts is available on the Instructions for Authors page. Cancers is an international peer-reviewed open access semimonthly journal published by MDPI.

Please visit the Instructions for Authors page before submitting a manuscript. The Article Processing Charge (APC) for publication in this open access journal is 2900 CHF (Swiss Francs). Submitted papers should be well formatted and use good English. Authors may use MDPI's English editing service prior to publication or during author revisions.

Keywords

  • venous thromboembolism
  • cancer
  • low molecular weight heparin
  • direct oral anticoagulant

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Published Papers (9 papers)

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Editorial

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5 pages, 196 KiB  
Editorial
Management of Cancer-Associated Thrombosis: An Evolving Area
by Corinne Frere, Jean M. Connors and Dominique Farge
Cancers 2020, 12(10), 2999; https://doi.org/10.3390/cancers12102999 - 16 Oct 2020
Cited by 1 | Viewed by 2516
Abstract
The management of cancer-associated thrombosis (CAT) is an evolving area. With the use of direct oral anticoagulants as a new option in the management of CAT, clinicians now face several choices for the individual cancer patient with venous thromboembolism. A personalized approach, matching [...] Read more.
The management of cancer-associated thrombosis (CAT) is an evolving area. With the use of direct oral anticoagulants as a new option in the management of CAT, clinicians now face several choices for the individual cancer patient with venous thromboembolism. A personalized approach, matching the right drug to the right patient, based on drug properties, efficacy and safety, side effect profile of each drug, and patient values and preference, will probably supplant the one size fits all approach of use of only low-molecular-weight heparin in the near future. We herein present eight translational, clinical research, and review articles on recent advances in the management of CAT published in the Special Issue “Treatment for Cancer-Associated Thrombosis” of Cancers. For now, a multidisciplinary patient-centered approach involving a close cooperation between oncologists and other specialists is warranted to guide clinical decision making and optimize the treatment of VTE in cancer patient. Full article
(This article belongs to the Special Issue Treatment of Cancer-Associated Thrombosis)

Research

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12 pages, 1201 KiB  
Article
Prognostic Significance of Incidental Deep Vein Thrombosis in Patients with Cancer Presenting with Incidental Pulmonary Embolism
by Maria Barca-Hernando, Rocio Ortega-Rivera, Sergio Lopez-Ruz, Teresa Elias-Hernandez, Maria Isabel Asensio-Cruz, Samira Marin-Romero, Javier Toral, Emilio Montero, Veronica Sanchez, Elena Arellano, Jose Maria Sanchez-Diaz, Macarena Real-Dominguez, Remedios Otero-Candelera and Luis Jara-Palomares
Cancers 2020, 12(8), 2267; https://doi.org/10.3390/cancers12082267 - 13 Aug 2020
Cited by 6 | Viewed by 2897
Abstract
In symptomatic acute pulmonary embolism (PE), the presence of deep vein thrombosis (DVT) is a risk factor for 30- and 90-day mortality. In patients with cancer and incidental PE, the prognostic effect of concomitant incidental DVT is unknown. In this retrospective study, we [...] Read more.
In symptomatic acute pulmonary embolism (PE), the presence of deep vein thrombosis (DVT) is a risk factor for 30- and 90-day mortality. In patients with cancer and incidental PE, the prognostic effect of concomitant incidental DVT is unknown. In this retrospective study, we examined the effect of incidental DVT on all-cause mortality in such patients. Adjusted Cox multivariate regression analysis was used for relevant covariates. From January 2010 to March 2018, we included 200 patients (mean age, 65.3 ± 12.4 years) who were followed up for 12.5 months (interquartile range 7.4–19.4 months). Of these patients, 62% had metastases, 31% had concomitant incidental DVT, and 40.1% (n = 81) died during follow-up. All-cause mortality did not increase in patients with DVT (hazard ratio [HR] 1.01, 95% confidence interval [CI] 0.43–2.75, p = 0.855). On multivariate analysis, weight (adjusted HR 0.96, 95% CI 0.92–0.99, p = 0.032), and metastasis (adjusted HR 10.26, 95% CI 2.35–44.9, p = 0.002) were predictors of all-cause mortality. In conclusion, low weight and presence of metastases were associated with all-cause mortality, while presence of concomitant DVT was unrelated to poorer survival. Full article
(This article belongs to the Special Issue Treatment of Cancer-Associated Thrombosis)
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16 pages, 3368 KiB  
Article
Primary Thromboprophylaxis in Ambulatory Pancreatic Cancer Patients Receiving Chemotherapy: A Systematic Review and Meta-Analysis of Randomized Controlled Trials
by Corinne Frere, Benjamin Crichi, Barbara Bournet, Cindy Canivet, Nassim Ait Abdallah, Louis Buscail and Dominique Farge
Cancers 2020, 12(8), 2028; https://doi.org/10.3390/cancers12082028 - 24 Jul 2020
Cited by 21 | Viewed by 3461
Abstract
Patients with pancreatic cancer (PC) carry the highest risk of venous thromboembolism (VTE) amongst all cancer patients. Appropriate use of primary thromboprophylaxis might significantly and safely reduce its burden. We performed a systematic review of published studies and meeting abstracts using MEDLINE and [...] Read more.
Patients with pancreatic cancer (PC) carry the highest risk of venous thromboembolism (VTE) amongst all cancer patients. Appropriate use of primary thromboprophylaxis might significantly and safely reduce its burden. We performed a systematic review of published studies and meeting abstracts using MEDLINE and EMBASE through July 2020 to evaluate the efficacy and safety of primary thromboprophylaxis in ambulatory PC patients receiving chemotherapy. The Mantel–Haenszel random effect model was used to estimate the pooled event-based risk ratio (RR) and the pooled absolute risk difference (RD) with a 95% confidence interval (CI). Five randomized controlled studies with 1003 PC patients were included in this meta-analysis. Compared to placebo, thromboprophylaxis significantly decreased the risk of VTE (pooled RR 0.31, 95% CI 0.19–0.51, p < 0.00001, I2 = 8%; absolute RD −0.08, 95% CI −0.12–−0.05, p < 0.00001, I2 = 0%), with an estimated number needed to treat of 11.9 patients to prevent one VTE event. Similar reductions of VTE were observed in studies with parenteral (RR 0.30, 95% CI 0.17–0.53) versus oral anticoagulants (RR 0.37, 95% CI 0.14–0.99) and in studies using prophylactic doses of anticoagulants (RR 0.34, 95% CI 0.17–0.70) versus supra-prophylactic doses of anticoagulants (RR 0.27, 95% CI 0.08–0.90). The pooled RR for major bleeding was 1.08 (95% CI 0.47–2.52, p = 0.85, I2 = 0%) and the absolute RD was 0.00 (95% CI −0.02–0.03, p = 0.85, I2 = 0%). Evidence supports a net clinical benefit of thromboprophylaxis in ambulatory PC patients receiving chemotherapy. Adequately powered randomized phase III studies assessing the most effective anticoagulant and the optimal dose, schedule and duration of thromboprophylaxis to be used are warranted. Full article
(This article belongs to the Special Issue Treatment of Cancer-Associated Thrombosis)
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11 pages, 1806 KiB  
Article
Single-Drug Approach with Edoxaban is Effective for Resolving Non-Acute Cancer-Associated Venous Thrombosis: A Single-Arm Retrospective Analysis
by Hirokazu Toshima, Atsushi Hisamatsu, Kouji Kobayashi, Hiroo Ishida and Ken Shimada
Cancers 2020, 12(7), 1711; https://doi.org/10.3390/cancers12071711 - 28 Jun 2020
Cited by 3 | Viewed by 2551
Abstract
Recently, cancer-related venous thromboembolism (VTE) has been termed “cancer-associated thrombosis (CAT)” and is the focus of current research. We retrospectively investigated the efficacy of a single-drug approach with edoxaban for the treatment of non-acute CAT. Thirty-two non-acute CAT patients who received edoxaban were [...] Read more.
Recently, cancer-related venous thromboembolism (VTE) has been termed “cancer-associated thrombosis (CAT)” and is the focus of current research. We retrospectively investigated the efficacy of a single-drug approach with edoxaban for the treatment of non-acute CAT. Thirty-two non-acute CAT patients who received edoxaban were analyzed. The primary endpoint of this analysis was the thrombus disappearance rate at the first evaluation. Secondary endpoints included progression/recurrence of VTE, major bleeding, and D-dimer levels. The thrombus disappearance rate was 62.5%. Therefore, the null hypothesis for the primary endpoint (thrombus disappearance rate of ≤32.0%) was rejected (p = 0.00038) based on the rate of the previous study as the historical control. Recurrent VTE and major bleeding occurred in two patients each. After the start of treatment with edoxaban, a significant difference in D-dimer levels was observed (p = 0.00655). We demonstrated that a single-drug approach with edoxaban is a potential treatment option for non-acute CAT. Full article
(This article belongs to the Special Issue Treatment of Cancer-Associated Thrombosis)
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19 pages, 1773 KiB  
Article
microRNAs and Markers of Neutrophil Activation as Predictors of Early Incidental Post-Surgical Pulmonary Embolism in Patients with Intracranial Tumors
by Julia Oto, Emma Plana, María José Solmoirago, Álvaro Fernández-Pardo, David Hervás, Fernando Cana, Francisco España, Andrea Artoni, Paolo Bucciarelli, Giorgio Carrabba, Silvia Navarro, Giuliana Merati and Pilar Medina
Cancers 2020, 12(6), 1536; https://doi.org/10.3390/cancers12061536 - 11 Jun 2020
Cited by 21 | Viewed by 3196
Abstract
Venous thromboembolism (VTE) is a common complication of cancer that severely increases morbidity and mortality. Patients with intracranial tumors are more likely to develop VTE than patients with cancers at other sites. Conversely, limited tools exist to identify patients with high thrombotic risk. [...] Read more.
Venous thromboembolism (VTE) is a common complication of cancer that severely increases morbidity and mortality. Patients with intracranial tumors are more likely to develop VTE than patients with cancers at other sites. Conversely, limited tools exist to identify patients with high thrombotic risk. Upon activation, neutrophils release their content through different mechanisms triggering thrombosis. We explored the ability of microRNAs (miRNAs) and plasma markers of neutrophil activation measured before surgery to predict the risk of early post-surgical pulmonary embolism (PE) in glioma and meningioma patients. We recruited and prospectively followed 50 patients with glioma and 50 with meningioma, 34% of whom in each group developed an early objectively-diagnosed post-surgical PE. We measured miRNA expression and neutrophil markers (cell-free DNA, nucleosomes, calprotectin and myeloperoxidase) before surgery. In glioma patients, we adjusted and validated a predictive model for post-surgical PE with 6 miRNAs: miR-363-3p, miR-93-3p, miR-22-5p, miR-451a, miR-222-3p and miR-140-3p (AUC = 0.78; 95% Confidence Interval (CI) [0.63, 0.94]) and another with cfDNA and myeloperoxidase as predictors (AUC = 0.71; 95% CI [0.52, 0.90]). Furthermore, we combined both types of markers and obtained a model with myeloperoxidase and miR-140-3p as predictors (AUC = 0.79; 95% CI [0.64, 0.94]). In meningioma patients we fitted and validated a predictive model with 6 miRNAs: miR-29a-3p, miR-660-5p, miR-331-3p, miR-126-5p, miR-23a-3p and miR-23b-3p (AUC = 0.69; 95% CI [0.52, 0.87]). All our models outperformed the Khorana score. This is the first study that analyzes the capability of plasma miRNAs and neutrophil activation markers to predict early post-surgical PE in glioma and meningioma patients. The estimation of the thrombotic risk before surgery may promote a tailored thromboprophylaxis in a selected group of high-risk patients, in order to minimize the incidence of PE and avoid bleedings. Full article
(This article belongs to the Special Issue Treatment of Cancer-Associated Thrombosis)
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Graphical abstract

15 pages, 1026 KiB  
Article
Genome-Wide Association Meta-Analysis of Single-Nucleotide Polymorphisms and Symptomatic Venous Thromboembolism during Therapy for Acute Lymphoblastic Leukemia and Lymphoma in Caucasian Children
by Marion K. Mateos, Morten Tulstrup, Michael CJ Quinn, Ruta Tuckuviene, Glenn M. Marshall, Ramneek Gupta, Chelsea Mayoh, Benjamin O. Wolthers, Pasquale M. Barbaro, Ellen Ruud, Rosemary Sutton, Pasi Huttunen, Tamas Revesz, Sonata S. Trakymiene, Draga Barbaric, Ulf Tedgård, Jodie E. Giles, Frank Alvaro, Olafur G. Jonsson, Françoise Mechinaud, Kadri Saks, Daniel Catchpoole, Rishi S. Kotecha, Luciano Dalla-Pozza, Georgia Chenevix-Trench, Toby N. Trahair, Stuart MacGregor and Kjeld Schmiegelowadd Show full author list remove Hide full author list
Cancers 2020, 12(5), 1285; https://doi.org/10.3390/cancers12051285 - 19 May 2020
Cited by 6 | Viewed by 4303
Abstract
Symptomatic venous thromboembolism (VTE) occurs in five percent of children treated for acute lymphoblastic leukemia (ALL), but whether a genetic predisposition exists across different ALL treatment regimens has not been well studied. Methods: We undertook a genome-wide association study (GWAS) meta-analysis for VTE [...] Read more.
Symptomatic venous thromboembolism (VTE) occurs in five percent of children treated for acute lymphoblastic leukemia (ALL), but whether a genetic predisposition exists across different ALL treatment regimens has not been well studied. Methods: We undertook a genome-wide association study (GWAS) meta-analysis for VTE in consecutively treated children in the Nordic/Baltic acute lymphoblastic leukemia 2008 (ALL2008) cohort and the Australian Evaluation of Risk of ALL Treatment-Related Side-Effects (ERASE) cohort. A total of 92 cases and 1481 controls of European ancestry were included. Results: No SNPs reached genome-wide significance (p < 5 × 10−8) in either cohort. Among the top 34 single-nucleotide polymorphisms (SNPs) (p < 1 × 10−6), two loci had concordant effects in both cohorts: ALOX15B (rs1804772) (MAF: 1%; p = 3.95 × 10−7) that influences arachidonic acid metabolism and thus platelet aggregation, and KALRN (rs570684) (MAF: 1%; p = 4.34 × 10−7) that has been previously associated with risk of ischemic stroke, atherosclerosis, and early-onset coronary artery disease. Conclusion: This represents the largest GWAS meta-analysis conducted to date associating SNPs to VTE in children and adolescents treated on childhood ALL protocols. Validation of these findings is needed and may then lead to patient stratification for VTE preventive interventions. As VTE hemostasis involves multiple pathways, a more powerful GWAS is needed to detect combination of variants associated with VTE. Full article
(This article belongs to the Special Issue Treatment of Cancer-Associated Thrombosis)
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12 pages, 578 KiB  
Article
Low Systemic Levels of Chemokine C-C Motif Ligand 3 (CCL3) are Associated with a High Risk of Venous Thromboembolism in Patients with Glioma
by Pegah Mir Seyed Nazari, Christine Marosi, Florian Moik, Julia Riedl, Öykü Özer, Anna Sophie Berghoff, Matthias Preusser, Johannes A. Hainfellner, Ingrid Pabinger, Gerhard J. Zlabinger and Cihan Ay
Cancers 2019, 11(12), 2020; https://doi.org/10.3390/cancers11122020 - 14 Dec 2019
Cited by 13 | Viewed by 3239
Abstract
A tight interplay between inflammation and hemostasis has been described as a potential driver for developing venous thromboembolism (VTE). Here, we investigated the association of systemic cytokine levels and risk of VTE in patients with glioma. This analysis was conducted within the prospective, [...] Read more.
A tight interplay between inflammation and hemostasis has been described as a potential driver for developing venous thromboembolism (VTE). Here, we investigated the association of systemic cytokine levels and risk of VTE in patients with glioma. This analysis was conducted within the prospective, observational Vienna Cancer and Thrombosis Study. Patients with glioma were included at time of diagnosis or progression and were observed for a maximum of two years. Primary endpoint was objectively confirmed VTE. At study entry, a single blood draw was performed. A panel of nine cytokines was measured in serum samples with the xMAP technology developed by Luminex. Results: Overall, 76 glioma patients were included in this analysis, and 10 (13.2%) of them developed VTE during the follow-up. Chemokine C-C motif ligand 3 (CCL3) levels were inversely associated with risk of VTE (hazard ratio [HR] per double increase, 95% confidence interval [CI]: 0.385, 95% CI: 0.161–0.925, p = 0.033), while there was no association between the risk of VTE and serum levels of interleukin (IL)-1β, IL-4, IL-6, IL-8, IL-10, IL-11, tumor necrosis factor (TNF)-α and vascular endothelial growth factor (VEGF), respectively. In conclusion, low serum levels of CCL3 were associated with an increased risk of VTE. CCL3 might serve as a potential biomarker to predict VTE risk in patients with glioma. Full article
(This article belongs to the Special Issue Treatment of Cancer-Associated Thrombosis)
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Review

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12 pages, 540 KiB  
Review
Incidence, Therapy, and Bleeding Risk—Cancer- Associated Thrombosis in Patients with Glioblastoma
by Viktoria Muster and Thomas Gary
Cancers 2020, 12(6), 1354; https://doi.org/10.3390/cancers12061354 - 26 May 2020
Cited by 13 | Viewed by 3587
Abstract
Cancer is an independent risk factor for the development of venous thromboembolism (VTE). Glioblastomas are amongst cancer types with the most thrombogenic potential and patients are at a particularly high risk of VTE with an incidence up to 20–30% per year. Currently, major [...] Read more.
Cancer is an independent risk factor for the development of venous thromboembolism (VTE). Glioblastomas are amongst cancer types with the most thrombogenic potential and patients are at a particularly high risk of VTE with an incidence up to 20–30% per year. Currently, major efforts are underway to gain novel insights into risk factors and pathomechanisms to provide a better understanding of development of VTE in patients with primary brain tumors. Treatment of VTE requires therapeutic anticoagulation, which accordingly to recently-published guidelines should be performed using low molecular weight heparin or, in case of low bleeding risk, using a direct oral anticoagulant. However, this can be very challenging due to an increased risk of intracranial hemorrhage in this patient group. Furthermore, limited data are available on the subgroup of patients with primary brain tumors. Full article
(This article belongs to the Special Issue Treatment of Cancer-Associated Thrombosis)
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Other

9 pages, 459 KiB  
Perspective
Are Patients with Active Cancer and Those with History of Cancer Carrying the Same Risks of Recurrent VTE and Bleeding While on Anticoagulants?
by Corinne Frere, Benjamin Crichi, Manon Lejeune, Jean-Philippe Spano and Nicolas Janus
Cancers 2020, 12(4), 917; https://doi.org/10.3390/cancers12040917 - 9 Apr 2020
Cited by 13 | Viewed by 4059
Abstract
Direct oral anticoagulants (DOAC) are now recommended for the treatment of cancer-associated thrombosis (CAT) based on the results of dedicated trials demonstrating that DOAC are non-inferior to low molecular weight heparins in preventing recurrent venous thromboembolism (VTE) in this population. The definition of [...] Read more.
Direct oral anticoagulants (DOAC) are now recommended for the treatment of cancer-associated thrombosis (CAT) based on the results of dedicated trials demonstrating that DOAC are non-inferior to low molecular weight heparins in preventing recurrent venous thromboembolism (VTE) in this population. The definition of “cancer patient” differs substantially among studies. Whether patients with active cancer and those with a history of cancer (HOC) carry the same risks of recurrent VTE and bleeding remains unclear. Few studies reported data on the efficacy and safety of anticoagulants according to active cancer or HOC categories. While in subgroup analyses of EINSTEIN and HOKUSAI the rates of recurrent VTE and bleeding did not differ between these categories, results from a subgroup analysis of AMPLIFY, from HOKUSAI-Cancer, and from the COMMAND cohort suggest that HOC patients might have a lower bleeding risk than active cancer patients. Whether the inclusion of HOC patients in CAT studies might introduce some bias by decreasing the rates of both recurrent VTE and bleeding remains an unanswered issue since no dedicated prospective study addressed this question. A strict definition of active cancer should be used in further trials. Full article
(This article belongs to the Special Issue Treatment of Cancer-Associated Thrombosis)
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