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Venous thromboembolism in patients undergoing pancreatic cancer surgery (PaTR-VTE) with curative intent; protocol of a prospective observational study

BMC Surgery volume 25, Article number: 183 (2025) Cite this article

Abstract

Background

Pancreatic cancer is probably the most thrombotic malignancy, with an incidence of venous thromboembolism (VTE) of up to 18%. However, the exact pathophysiological mechanisms involved in the development of VTE in the setting of pancreatic cancer are not yet well understood. The primary endpoint of the study is to evaluate the neutrophil/lymphocyte ratio (NLR) and other coagulation biomarkers as predictors of VTE in patients with pancreatic cancer undergoing surgery with curative intent. The exact incidence of VTE, perioperative coagulation status of patients and the possible determinants of VTE in the aforementioned population are the secondary study objectives.

Methods

This prospective, non-interventional observational study is conducted according to the STROBE concept. It has been approved by the ethical committee and registered (NCT05964621) and will include eligible patients with primary pancreatic cancer with resectable or borderline resectable disease undergoing surgery with curative intent. Exclusion criteria are: Refusal to participate, previous thromboembolic event < 6 months, ASA score > 3, patients deemed inoperable intraoperatively and the concurrent presence of a second primary malignancy. Three blood samples are taken from all patients (preoperatively, immediately after the operation, and before discharge) and the serum values of the following parameters are determined: Haemoglobin, white blood cells, INR, liver and kidney function tests, von Willebrand factor, factors VIII and XI, D-dimers, fibrinogen, platelet function, Adamts 13 and anti-Xa. One month after the procedure, scheduled screening for asymptomatic deep vein thrombosis (DVT) is performed with a lower extremity ultrasound triplex study. In addition, thromboembolic events (DVT, pulmonary embolism (PE)) diagnosed during the hospital stay period are recorded. Low molecular weight heparin will be routinely administered from the first postoperative day, with the dosage, i.e. prophylactic or therapeutic titrated according to the patient’s history of cardiovascular disease. According to the literature, the pooled specificity of the admission NLR for 30-day VTE and PE prediction is 80.5%, while the VTE rates after pancreatectomy is 1.5%. Based on a 95% confidence level and a precision of 0.1, the estimated sample size for the specificity outcome is 62 patients.

Discussion

The aim of this study is to identify predictors of postoperative VTE in patients undergoing pancreatic cancer surgery. The results could lead to an optimization of perioperative care.

Trial registration

NCT05964621. Registered on July, 2023 clinicaltrials.org.

Peer Review reports

Background and rationale

Cancer-associated thrombosis (CAT) is the second most common cause of death in oncology patients after the progression of the tumour itself. This patient group has an increased risk of both venous (4–20%) and arterial (2–5%) thromboembolic events. Cancer is probably the most important acquired risk factor for the development of venous thromboembolism (VTE). The incidence of CAT varies according to tumour type, tumour stage and type of therapy. The aetiology appears to be multifactorial. The progression of the disease and the various forms of therapeutic interventions, such as chemotherapy, hormone therapy or surgery all played a role. Nevertheless, the specific type of tumour, the overall tumour burden as well as with the various parameters influencing the tumour microenvironment, remain the most important modulators of thrombosis risk in cancer patients [1,2,3].

Pancreatic cancer is the fourth most lethal cancer worldwide and probably the most thrombogenic with an incidence of VTE between 8 and 18% [4]. Although the exact pathophysiological mechanisms are still not fully understood, pancreatic cancer appears to cause hypercoagulation. Specifically, it has been postulated that pancreatic cancer cells have certain intrinsic properties that enable them to activate platelets. The activated platelets degranulate and release proinflammatory molecules that attract neutrophils in the tumour microenvironment and promote various thrombogenic processes [5].

In addition, neutrophils further amplify local tumour-induced inflammation by switching to the “pro-tumoural N2 phenotype”. These “N2” neutrophils enhance CAT by either secreting neutrophil extracellular traps that intercept platelets and coagulation factors or by expressing procoagulant molecules such as P-selectin and tissue factor. Tumour cells produce and release several proinflammatory cytokines that further contribute to the hypercoagulation in malignancy. Furthermore, the induced inflammation seems to enhance the effect of induced fibrinolysis. Pancreatic cancer cells express thrombin and interact directly with the protease-activated receptors (PAR) of platelets, leading to their activation. Thrombin may in turn indirectly interact with various coagulation factors, while platelets may contribute to vascular endothelial dysfunction and von Willebrand factor (vWF) abnormalities [1,2,3]. Literature reports have highlighted white blood cell count and neutrophil-to-lymphocyte ratio (NLR) as predictors of acute pulmonary embolism in oncology patients [4, 6].

The relationship between cancer, coagulation and inflammation appears to be quite complex and poorly defined [1,2,3,4, 6]. Neutrophils for example, can promote tumour growth but also have anti-metastatic and cytotoxic properties. Lymphocytes are of paramount importance for the anti-tumour immune response, but are largely absent in the pancreatic ductal adenocarcinoma (PDAC) microenvironment [6]. Overall, PDAC appears to be able to activate the local release of proinflammatory and prothrombotic factors.

Despite the considerable progress in all areas of cancer treatment, the prognosis of pancreatic cancer remains poor, as most patients are only diagnosed at an advanced stage. Only 10 to 20% of patients are diagnosed at an earlier stage. For these patients, treatment options include surgery, radiotherapy and chemotherapy, and if these therapies are combined in the right way, the results can be favourable and even lead to a cure. Pancreatic cancer is classified as resectable, borderline resectable and non-resectable depending on the relative relationship of the tumour with the major peripancreatic vascular structures and the presence of metastases.

According to the guidelines of the European Society of Medical Oncology, early surgical resection in combination with adjuvant chemotherapy remains the optimal therapeutic approach for resectable pancreatic cancer while surgery after neoadjuvant chemotherapy is suggested for borderline resectable cancer [6,7,8]. Unfortunately, even after optimal therapy, PDAC is characterized by poor disease-free survival of about 15–19 months. The often early recurrence of disease after treatment and pancreatic cancer-related complications such as venous thromboembolism are the cause of the poor outcomes and emphasize the need for improved patient risk stratification and targeted interventions that could prevent these potentially fatal complications. NLR is an-easy-to calculate and inexpensive biomarker that has been significantly associated with poor prognosis and lower survival rates in various malignancies such as rectal and small cell lung cancer. In PDAC, its benefit is limited only in advanced, metastatic disease. In resectable PDAC, CA 19–9 values, with their inherent limitations and certain pathologic features of the resected specimen, such as the status of the resection margin, have been used for prognostic purposes. [6, 9]. Thus, if the prognostic significance of preoperative NLR values for early postoperative VTE could be confirmed, this would have direct implications for patient management, stratification of VTE-risk and optimal individualized patient care.

Objective

The primary endpoint of this study is to assess the predictive value of, preoperatively or early postoperatively, NLR for VTE in patients with pancreatic cancer undergoing surgery. We also investigated: (i) the incidence of VTE (ii) the perioperative coagulation status of pancreatic cancer patients (iii) the predictive value of coagulation biomarkers/parameters for VTE and (iv) the possible determinants or predictive factors for VTE in the baseline characteristics of patients in the given patient group.

Study design

This prospective single-centre, non-interventional observational study will follow the Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) guidelines [10].

Methods/design

Setting of the study

This prospective non-interventional observational, study will be conducted at a tertiary centre, Larissa University Hospital (UHL). The study schedule and data collection are summarised in Fig. 1.

Fig. 1
figure 1

Overview of study timeline and data collection. GA: General Anaesthesia; PACU: Post-anaesthesia Care Unit; DVT: Deep Vein Thrombosis; LMWH: Low Molecular Weight Heparin; INR: International Normalized Ratio

Full size image

Criteria for participation

Participants

Consecutive patients with pancreatic cancer undergoing surgery with curative intent will be included. All patients will be followed up for 30 days. In general, patients with primary pancreatic cancer will be appropriately staged according to the National Comprehensive Cancer Network (NCCN) guidelines version 2.2023 [11], with high quality imaging.

Data collection

Consecutive

Inclusion criteria

 1. Age > 18 years

 2. Patients suffering from pancreatic cancer undergoing pancreatic cancer resection in University Hospital of Larissa

Exclusion criteria

 1. Refuse to participate

 2. Previous thromboembolic event < 6 months prior to the operation

 3. History of inherited or acquired bleeding disorder

 4. American Society Anaesthesiologist Physical Status (ASA PS) > 3

 5. Concomitant presence of a second primary malignancy

 6. Unresectable pancreatic cancer

Interventions

Standard perioperative care

Perioperative care is provided in accordance with institutional guidelines and the updated recommendations for enhanced recovery after surgery (ERAS) [12]. As patients with borderline resectable pancreatic cancer are at high risk of a positive resection margin, neoadjuvant chemotherapy is given to these patients prior to resection. In contrast, patients with resectable disease are treated with an upfront resection. Depending on the location of the tumour within the pancreatic parenchyma, a pancreaticoduodenectomy, a distal pancreatectomy or even a total pancreatectomy is performed. All operations are performed via an open approach. If there is venous involvement, a lateral venorrhaphy or a complete resection and reconstruction of the portal vein or the superior mesenteric vein is performed. In Whipple’s procedure, we routinely aim to preserve the pylorus while performing a pancreaticojejunostomy to restore continuity of the gastrointestinal tract continuity. Anaesthesia and perioperative management are routinely performed by the attending anaesthesiologistt according to the updated ERAS [12] and multimodal analgesia guidelines [13, 14]. In cases, epidural analgesia will be administered if deemed appropriate. Transfusion of blood and blood products will be guided by point-of-care testing (thromboelastography) and at the discretion of the attending anaesthesiologist and surgeon, during or after surgery. Low-molecular-weight-heparin will be routinely administered from the first postoperative day, with the dosage, i.e. prophylactic or therapeutic titrated according to the patient’s history of cardiovascular disease.

Outcomes

Evaluation and treatment of venous thromboembolism

The evaluation and treatment of venous thromboembolism, including deep vein thrombosis and pulmonary embolism and asymptomatic DVT at 30-day follow-up, is performed according to the updated guidelines of the American Society of Hematology [15] and the European Cardiology and Respiratory Societies [16].

Blood samples

Perioperative laboratory tests are performed according to institutional guidelines. These include a complete blood count, conventional coagulation tests, liver and renal function tests. In addition, the following parameters will also be determined for the purposes of this study; vWF, factors VIII and XI, D-dimers, fibrinogen, platelet activation (multiplate), Adamts 13, anti-Xa and high-sensitivity troponin. All samples are taken by puncture of a peripheral vein. Blood samples are taken at three time points: preoperatively before induction of general anaesthesia, early postoperatively immediately after admission of the patient to the post-anaesthesia-care-unit (PACU) and late postoperatively (10th postoperative day). All blood samples are taken at least 12 h after the administration of low molecular weight heparin (LMWH) to minimise any anticoagulant effects on the laboratory tests. The anti-Xa value is also determined to rule out any anticoagulant effects on the laboratory tests.

Data collection

Most of the data is obtained from the routine admission documents and the electronic patient file. They are recorded in a password-protected spreadsheet.

Basic data collection

 1. Demographics: age, gender, ethnic origin

 2. Comorbidities and administrated drug therapy

 3. ASA PS

 4. Lifestyle: smoking status, alcohol intake, level of physical activity, body mass index

 5. Tumour-related history: date of malignancy diagnosis and any-tumour related administrated therapy

 6. Any previous VTE episodes

 7. Perioperative history: date of tumour resection, type of surgery, duration of surgery, anaesthesia plan (general anaesthesia, epidural analgesia, intravenous lidocaine or dexmedetomidine administration), type of intravenous fluids administration

 8. Length of hospital stay

 9. Time of first dose of low molecular weight heparin

 10. Any complication during hospital staya

  1. aThe definition and grading from the International Study Group for Pancreatic Surgery (ISGPS), along with the Clavien-Dindo classification and the Comprehensive Complication Index (CCI) will be also used for the record and classification of complications [17,18,19]

Laboratory values assessed as possible VTE predictors

 1. NLR

 2. vWF

 3. Factor VIII

 4. Factor XI

 5. D-dimers

 6. Fibrinogen

 7. Adamts 13

 8. Platelet function (multiplate R)

VTE manifestations

 1. Deep vein thrombosis

 2. Pulmonary embolism

 3. Asymptomatic deep vein thrombosis (DVT) at 30 days follow-up

Statistical methods

Sample size

According to the literature, the pooled specificity of admission NLR for the 30-day prediction of VTE and PE is 80.5% [9]. The VTE rate after pancreatectomy is 1.5% [20]. Based on a 95% confidence level and a 0.1 precision, the estimated sample size for the specificity result is 62 patients. To counteract for possible dropouts, the sample size was increased to 70 patients.

Statistical analysis

Categorical variables (demographics, comorbidities, polypharmacy, ASA score, etc.) will be expressed as n and percentage (%) and continuous variables (age) as mean ± standard deviation. Categorical variables will be analysed using chi-square or Fisher exact test. All normally distributed continuous variables will be assessed with the Student’s T-test or ANOVA test, and for the non- normally distributed variables, the non-parametric Kruskal- Wallis test will be used on a rank basis to determine statistical significance between the different groups.

The association between potential/possible prognostic or VTE predictors and prognosis or VTE disease manifestations will be analysed using a regression model and adjusted for confounding factors. Sensitivity and specificity analyses are performed using the Receiver Operating Characteristic Curve (ROC). A p-value of < 0.05 will be considered statistically significant. SPSS16 will be used for statistical analysis (IBM Corp, Released 2013, IBM SPSS Statistics).

Ethics and dissemination

All patients are informed orally and in writing. In accordance with the Declaration of Helsinki, written informed consent is obtained from all participating patients [21]. For patients who are unable to give informed consent, their next of kin will provide informed consent [21]. The participants data will be pseudo-anonymized with a study identification (ID) [10]. The study was registered at clinicaltrials.org (NCT05964621, registered on July, 2023).

Discussion

The aim of this study is to determine the clinical utility and predictive value of preoperative or early postoperative NLR values or coagulation biomarkers/parameters, such as vWF or Adamts-13 for the early postoperative occurrence of VTE in patients with pancreatic cancer undergoing resection with curative intent. In addition the incidence of VTE in patients with primary resectable pancreatic cancer and possible determinant of VTE among coagulation parameters or baseline characteristics of patients will be investigated. The fact that the study is conducted at a single centre and the fact that certain laboratory values are assessed should be considered the main limitations of the study. However, to the best of our knowledge, this is the first study to investigate certain coagulation factors, such as Adamts-13 in the perioperative setting in pancreatic cancer. In summary, the results of the present study could optimize perioperative care in pancreatic cancer surgery.

Trial status

Protocol version number 27367/12–06-2023

Start of date recruitment—09/2023

Trial register: NCT05964621. Registered on July, 2023 clinicaltrials.org

Data availability

No datasets were generated or analysed during the current study.

Abbreviations

DVT:

Deep vein thrombosis

CAT:

Cancer associated thrombosis

VTE:

Venous thromboembolism

NLR:

Neutrophil to lymphocyte ratio

PAR:

Platelets’ protease-activated receptors

vWF:

Von Willebrand factor

PDAC:

Pancreatic ductal adenocarcinoma

UHL:

Larissa University Hospital

STROBE:

Strengthening the Reporting of Observational Studies in Epidemiology guidelines

ID:

Identification

ASA PS:

American Society Anaesthesiologist Physical Status

GA:

General anaesthesia

PACU:

Post-anaesthesia Care Unit

DVT:

Deep Vein Thrombosis

LMWH:

Low Molecular Weight Heparin;

INR:

International Normalized Ratio

NCCN:

National Comprehensive Cancer Network

ERAS:

Enhanced recovery after surgery

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Authors and Affiliations

  1. Department of Anaesthesiology, Faculty of Medicine, School of Health Sciences, University of Thessaly, Larissa University Hospital, Thessaly, Greece

    Maria P. Ntalouka & Eleni M. Arnaoutoglou

  2. Department of Surgery, Faculty of Medicine, School of Health Sciences, University of Thessaly, Larissa University Hospital, Thessaly, Greece

    Dimitrios Symeonidis, Konstantinos Tepetes & Dimitrios Zacharoulis

  3. Department of Transfusion Medicine, Faculty of Medicine, School of Health Sciences, University of Thessaly, Larissa University Hospital, Thessaly, Greece

    Paraskevi Kotsi

  4. Department of Microbiology, Faculty of Medicine, School of Health Sciences, University of Thessaly, Larissa University Hospital, Thessaly, Greece

    Efthymia Petinaki

  5. Department of Vascular Surgery, Faculty of Medicine, School of Health Sciences, University of Thessaly, Larissa University Hospital, Thessaly, Greece

    Miltiadis Matsagkas

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Contributions

EMA and MPNt conceived the original study and design. EMA, KT, DZ, MM, PK, EP, MPNt and DS were major contributors to the study design. EMA, KT and DZ will supervise the study. PK, EP, MM, KT, DZ and EMA led the protocol development, contributed to study design and analyzed data. MPNt and DS are responsible for data collection, data recording and preparing the manuscript. All authors have read and approve the final manuscript.

Corresponding authors

Correspondence to Maria P. Ntalouka or Dimitrios Symeonidis.

Ethics declarations

Ethics approval and consent to participate

Ethical approval was granted on 12/06/2023 by the Ethics Committee of the University Hospital of Larissa (27367). Written informed consent will be obtained from all participants or their next of kin. All methods will be performed in accordance with the Declaration of Helsinki.

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Not applicable.

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The authors declare no competing interests.

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Ntalouka, M.P., Symeonidis, D., Kotsi, P. et al. Venous thromboembolism in patients undergoing pancreatic cancer surgery (PaTR-VTE) with curative intent; protocol of a prospective observational study. BMC Surg 25, 183 (2025). https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s12893-024-02665-z

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