The incidence and risk factors of venous thromboembolism in patients with pancreatic cancer: a systematic review and meta-analysis

Introduction

Pancreatic cancer (PC) is extremely malignant and has the worst prognosis of all malignant tumors (1). PC is the third leading cause of cancer-related deaths and its incidence has gradually increased since cancer mortality has been reported (2). There are no specific symptoms in the initial stage, and about 50% of patients are in the local advanced stage or with metastases when diagnosed (3), and the median survival is less than 1 year (2).

Cancer-associated thromboembolism (CAT) is a common complication of malignant tumors and one of the main causes of death. It is closely related to the poor prognosis of patients and seriously affects their quality of life (4,5). Venous thromboembolism (VTE) is the most common form of CAT (6). VTE includes deep vein thrombosis and pulmonary embolism. Patients with cancer account for more than 20% of all newly diagnosed VTE cases (7). Notably, among all solid tumor malignancies, the incidence of cancer-related thrombosis remains high in patients with PC (8). It has been reported that the incidence of VTE in PC may be up to four times higher than that in other cancers (9).

The mechanism of VTE in PC is complicated, and related risk factors remain unclear. In addition to the genetic and innate biological characteristics of the tumor (8,10), other independent risk factors for VTE, such as chemotherapy, age, complications such as cardiovascular disease, cancer-related surgery, and tumor stage, further increase the risk of cancer-related VTE (11).

According to relevant studies, the incidence of VTE in patients with PC varies significantly among different studies (12,13). In addition, there is no consistent conclusion regarding the risk factors for VTE in patients with PC (14). Therefore, this study systematically reviewed existing cohort studies and case-control studies to explore the incidence and risk factors of VTE in patients with PC. We present this article in accordance with the MOOSE reporting checklist (15) (available at https://jgo.amegroups.com/article/view/10.21037/jgo-2025-132/rc).

Methods

The study protocol has been registered with the International System Review Registry Platform (PROSPERO) (registration No. CRD 42025645869).

Search strategy

Based on Patient/Population, Intervention, Comparison, Outcome (PICO) principles, we used medical subject headings (MeSH) terms supplemented by keywords, title, or abstract terms, and Boolean logic operations. We searched the literature from PubMed, EMBASE, Web of Science, Cochrane Library Central, China National Knowledge Infrastructure (CNKI), Wan Fang, and Vip databases from inception until December 25, 2024. PubMed’s MeSH term explosion and Embase’s EMTREE tree expansion were utilized to optimize search strategy. To ensure the comprehensiveness of the search, we manually checked reference lists of all included studies and contacted corresponding authors of potentially eligible trial to identify additional relevant literature. The terms included (pancreatic neoplasms OR pancreatic cancer) AND (thromboembolism OR venous thromboembolism OR deep vein thrombosis OR pulmonary embolism). The systematic search was conducted by two systematically trained researchers (H.X. and X.B.) with prior experience in systematic reviews, and the search strategy was peer-reviewed by the research team.

Selection criteria

The inclusion criteria were: (I) adults over 18 years of age with histopathologically diagnosed PC; (II) the incidence or risk factors of VTE associated with PC were reported; and (III) the study was designed as a cohort or case-control study. The exclusion criteria included (I) duplicate publications or lack of access to the full manuscript text; (II) studies where original data could not be retrieved; (III) conference abstracts, case reports, reviews, letters, comments, and expert opinions; and (IV) we excluded studies published in languages other than Chinese or English.

Study selection and data extraction

The retrieved literature was imported into Endnote21, and duplicates were removed. Two investigators independently screened the literature based on the criteria. Whenever disagreements arose, they were resolved by consulting with the third investigator or by reaching a consensus through group discussion. In addition, we systematically contacted the authors of three potentially eligible studies via email, yet received no responses regarding data availability or study eligibility clarification. Data were extracted from the included studies and recorded in a pre-designed characteristics table featuring the name of first author, publication year, country, sample, design, male-female ratio, tumor stage, age, therapy, complications, incidence of VTE, and median follow-up time.

Quality appraisal

Two investigators independently assessed the quality of the selected studies. For the included studies, the Newcastle-Ottawa scale (NOS) (16) was used to evaluate bias risk, focusing on selection, comparability, and exposure measurement. The NOS includes eight items with a potential total of 9 points, categorizing studies as low (0–3 points), moderate (4–6 points), or high quality (7–9 points). Discrepancies were resolved by consultation with a third author.

Statistical analysis

We summarized the incidence of VTE in PC patients. Odds ratio (OR) and 95% confidence interval (CI) were used to report risk factors for the incidence of VTE in patients with PC. If the study does not report ORs, it is directly extracted from the published contingency tables in the original study for calculation. When both multivariate and univariate outcome analyses were available, we chose the multivariate analysis after adjusting for confounders. Statistical significance was set at P<0.05. For heterogeneity testing, a fixed-effects model was applied if the heterogeneity was acceptable (P>0.1, I²<50%); otherwise, a random-effects model was employed. Meta-analyses were performed using the software Stata14.0 (StataCorp LLC, College Station, TX, USA), with results presented in forest plots. If data could not be included in the analysis, only descriptive analyses were conducted. Subgroup analysis was performed according to region, age, whether surgery was performed, whether distant metastasis occurred, comorbidities, and follow-up time. Sensitivity analysis was used to explore the impact of each study on the pooled results of the meta-analysis. Publication bias was assessed using funnel plots and Egger’s test.

Results

Search process

An initial search of electronic databases yielded 4,035 articles. After removing 772 duplicates using Endnote21, 3,263 articles remained. Screening titles and abstracts excluded 3,090 articles that did not meet the inclusion criteria. After a full-text review, 61 studies were included in this review. This process was shown in Figure 1.

Figure 1 Literature screening process and results. CNKI, China National Knowledge Infrastructure.

Characteristics of the included studies

The 61 included studies were published between 2005 and 2025 and conducted across 16 countries. This study included 53 cohort studies and 8 case-control studies with a combined sample size of 29,921 participants, predominantly male, and ages ranging from 54.2 to 75 years. The incidence of preoperative frailty ranged from 1.56% to 44.68%. Overall, the studies included were of moderate-to-high quality. Key characteristics are summarized in Table 1.

Meta-analysis results

Incidence of VTE in patients with PC

All included studies reported the incidence of VTE in patients with PC. Due to the high heterogeneity (I²=97.0%, P<0.01), a random effects model was adopted. The results showed that the incidence of VTE was 15.6% (95% CI: 13.7–17.6%) (Figure 2).

Figure 2 Incidence of VTE in patients with PC. CI, confidence interval; DL, DerSimonian and Laird; PC, pancreatic cancer; VTE, venous thromboembolism.

Subgroups were analyzed by region, age, comorbidity, whether surgery was performed, median follow-up time, and whether distant metastasis occurred. Due to the high heterogeneity among subgroups (I²>50%, P<0.1), random effects model was used.

There were 25 studies from Europe (n=10,162), 24 from Asia (n=8,972), and 12 from the United States (n=10,787). The incidence of VTE was 18% in Europe, 19% in the United States, and 11% in Asia. The included studies were grouped according to the average age of the patients. Patients older than 65 years had a higher incidence of VTE (18% vs. 16%). Patients were grouped according to different comorbidity. The results showed that the incidence of VTE was 20% in patients with coronary heart disease, 14% in diabetes, 15% in hypertension, and 7% in chronic obstructive pulmonary disease (COPD). A total of 18 studies reported median follow-up time. The incidence of VTE was 14% in patients with a median follow-up of more than 1 year and 11% in patients with a median follow-up of less than 1 year. Patients were grouped according to whether or not their tumors developed distant metastases. The incidence of VTE was 20% in patients with distant metastasis and 14% in patients without metastasis. Patients with PC who underwent resection had a higher incidence of VTE compared to those only received adjuvant therapy. The detailed results of subgroup analyses are shown in Table 2.

Risk factors for VTE in patients with PC

We conducted a meta-analysis of factors with a number of studies greater than or equal to 2, including a total of 5 factors. The results showed that patients whose tumors were located in the body and tail of the pancreas had a higher risk of VTE than those in the head of the pancreas (OR =1.92; 95% CI: 1.25–2.94). Poorly differentiation (OR =2.54; 95% CI: 1.53–4.23), tumor, node, metastasis (TNM) stage IV (OR =2.82; 95% CI: 1.12–7.08), and distant metastasis (OR =2.16; 95% CI: 1.59–2.93) also increased the risk of VTE in patients with PC. In addition, the increase of D-dimer after surgery (OR =4.33; 95% CI: 1.26–14.86) had a significant effect on the incidence of VTE (Figure 3). For the calculation of OR and 95% CI in the study of Chen et al. (17), please refer to Appendix 1.

Figure 3 Risk factors for VTE in patients with PC. CI, confidence interval; DL, DerSimonian and Laird; PC, pancreatic cancer; TNM, tumor node metastasis; VTE, venous thromboembolism.

Sensitivity analysis and publication bias

We performed sensitivity analyses by excluding studies one by one from the analysis. The results demonstrated that the combined effect size consistently fell within the overall 95% CI, confirming the stability of the findings. The funnel plot and Egger’s test results indicate that there is a certain publication bias (t=5.24; P<0.01) (Figure 4,5). After adding 26 studies using trim and fill analysis, we found that the adjusted incidence of VTE was 8% (95% CI: 0.59–0.10; P<0.01). This was not significantly different from before adjustment (95% CI: 0.14–0.18; P<0.01), indicating that publication bias had no significant effect on the results.

Figure 4 Funnel plot for publication bias. ES, effect size.

Figure 5 Egger test plot of publication bias in the included studies. CI, confidence interval; SND, standard normal deviate.

Discussion

This study comprehensively analyzed the incidence of VTE and risk factors in patients with PC, including 61 studies involving 29,921 patients. The included studies were rated as medium to high quality. The results showed that the incidence of VTE in patients with PC was 15.6%. Body or tail location, poorly differentiated, stage IV cancer, distant metastasis, and postoperative high level of D-dimer are risk factors for VTE.

To our knowledge, this is the first meta-analysis of the incidence and risk factors of VTE in patients with PC. This study focused on patients with PC, a high-risk group. Patients with PC have a significantly higher risk of VTE than patients with other cancers due to the impact of the disease itself and treatment, so the study of this group has important clinical significance. We not only focused on the incidence of VTE, but also delved into multiple potential risk factors. This helps identify high-risk patients and provides the basis for individualized prevention and management strategies

Our study has some limitations. First, the studies we included were all cohort or case-control studies, which can lead to bias. Second, significant heterogeneity was observed across included studies, likely due to variations in patients, and methods of VTE detection. Third, due to limited information, we did not have a specific classification of VTE. In addition, although we included a large number of studies, we did not have sufficient data to delve into more risk factors for VTE, such as genes and surgical methods. Moreover, our study excluded literature in other languages and unpublished articles, which limited the comprehensiveness of our analysis. Finally, despite thorough searches of major electronic databases, some studies were not included because they were incomplete or the full text was not available. Therefore, the results of this study should be interpreted with caution.

The incidence of VTE in patients with PC is much higher than that in the general population, as well as in patients with other types of cancer (73-76). This may be related to pancreatic tumor microenvironment, hypercoagulable state, and antitumor therapy (8). A study has shown that approximately 7.4% of patients with PC will develop VTE within 1 year of diagnosis, while the overall risk for patients with cancer is 3.1% (77). Our study showed that the incidence of VTE in patients with PC varied by region, age, comorbidities, and tumor metastasis. For example, studies in Asia have reported a lower incidence than in the United States and Europe. This may be related to differences in genetics, eating habits, and medical practices. This finding is similar to the results of previous studies (75,77,78). In addition, patients with chronic diseases, especially cardiovascular disease, have a significantly increased risk of VTE. These findings suggest that clinicians should develop individualized prevention strategies. However, many risk factors are associated with the patients themselves, and further confirmation of these uncontrollable factors is of little value to this study. The main research direction should be the optimization of controllable risk factors related to treatment and care. In addition, we found that patients who underwent resection had a higher incidence of VTE than those who received adjuvant therapy only. This finding is consistent with the results of previous research (38). VTE is the leading cause of postoperative morbidity and mortality in PC patients. In addition, the study has reported that the long operation time, multiple organ resection and minimally invasive surgery may be risk factors for VTE (58). However, owing to the difficulty of early diagnosis of PC and the high degree of malignancy, relatively few patients can undergo radical surgery. In the future, it will be necessary to further explore the influence of different surgical types and approaches.

The factors associated with VTE in patients with PC are multifaceted and complex. Due to limited data, we mainly analyzed the effect of tumor location and malignancy on the incidence of VTE. Biologically, tissue factor (TF) expressed on tumor cells, plasma components, and circulating microvesicles, along with thrombin-antithrombin (TAT) complexes, constitute the principal drivers of thrombogenesis in PC patients (79). Notably, elevated plasma TF levels not only critically mediate cancer-associated hypercoagulability but also represent an independent risk factor for VTE in this population (80). According to the analysis, patients with body and tail PC have a higher risk of VTE than those with tumors located at the head of the pancreas. This may be related to the fact that tumors in the body and tail of the pancreas usually do not obstruct of the pancreatic and bile ducts. Moreover, the onset of the disease is more insidious and difficult to find, and most patients have local or distant metastases during treatment (10,55). At this stage, patients typically exhibit elevated TF and TAT levels, which may further increase the risk of VTE (81). In addition, Frere et al. (12) found that the location of tumors in the isthmus was an independent predictor of VTE. Studies have shown that the risk of VTE increases with increasing tumor stage (82-84), and tumor metastasis is also an important risk factor for VTE in patients (12,42). These findings were consistent with our conclusions. This is because the D-dimer level in patients is related to tumor size, and the average size of the primary tumor in patients with metastasis is significantly larger and affected by tumor compression, which may increase the risk of VTE (83).

Several studies have reported that the incidence of VTE in patients with PC may be related to body mass index (BMI) (7,9,24,32,38,55,67). A study in Taiwan of patients with lung, stomach, and PCs, as well as lymphoma, reported that patients with very low or very high BMI levels had a higher risk of developing VTE (38). A Japanese study of VTE in PC patients reported significantly more VTE patients with BMI (≥25 kg/m²) (67). In patients undergoing surgery for PC, Eurola et al. found that high BMI (≥30 kg/m²), prior anticoagulant therapy, and disease recurrence were risk factors for VTE (7). In addition, the effects of old age (22), blood type (55), smoking (24), alcohol consumption (72), tumor size (24,32,55), chemotherapy (31), and other factors have been reported in previous studies. However, due to the limitations of the data provided in the articles, we did not conduct a meta-analysis.

In the future, relevant studies can be carried out to deepen our understanding of VTE in patients with PC and to optimize clinical management. First, research into different gene mutations (33) could uncover their role in thrombus formation, helping to identify high-risk patients and guide personalized prevention strategies. Second thrombus formation sites (e.g., deep vein thrombosis vs. pulmonary embolism) (14) may reveal patterns linked to disease progression or treatment outcomes, enabling targeted surveillance and early intervention. In addition, comparative studies on different thrombolytic schemes (8) are needed to evaluate their efficacy and safety, informing optimal treatment protocols. Furthermore, analyzing the impact of surgical paths (85) on VTE incidence could improve surgical planning and perioperative care. Finally, studies focusing on prognosis, including overall survival (72) or quality of life, are essential to understand the long-term effects of VTE on PC patients. By addressing these aspects, future research can provide a more comprehensive understanding of VTE in this high-risk population, leading to improved prevention, diagnosis, and treatment strategies.

Conclusions

The incidence of VTE is high in patients with PC. The tumor located in the body or tail, the degree of differentiation, stage IV cancer, distant metastasis, and postoperative high D-dimer levels are risk factors for VTE. Although the mixture of factors such as genetics or therapeutic regimen cannot be completely ruled out, the results still suggest that early identification of high-risk patients should be carried out in clinical work, and attention should be paid to the evaluation and intervention of VTE in PC patients, which may be conducive to improving the prognosis and quality of life of patients.

Acknowledgments

None.

Footnote

Reporting Checklist: The authors have completed the MOOSE reporting checklist. Available at https://jgo.amegroups.com/article/view/10.21037/jgo-2025-132/rc

Peer Review File: Available at https://jgo.amegroups.com/article/view/10.21037/jgo-2025-132/prf

Funding: None.

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://jgo.amegroups.com/article/view/10.21037/jgo-2025-132/coif). The authors have no conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

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