Abstract
Objective
To compare the diagnostic performance of pancreatic lesions using percutaneous ultrasound (US)-guided core needle biopsy (CNB) with and without contrast-enhanced ultrasound (CEUS).
Method
The patients were divided into two groups, US and CEUS group, based on whether CEUS was performed prior to biopsy. Before and after propensity score matching (PSM), the CNB-relevant characteristics of the two groups, including the first puncture success rate, the number of sampling, complication rate, type of complications, and degree of abdominal pain, were compared. The accuracy, sensitivity, specificity, positive predictive value (PPV), negative predictive value (NPV), and area under the curve (AUC) of percutaneous US-guided CNB were compared between the groups.
Results
This study included 277 patients (173 men and 104 women) with pancreatic lesions who underwent percutaneous CNB before PSM; 190 patients in the CEUS group, and 87 in the US group prior to CNB. After controlling for potential biases using PSM, no significant differences were observed in the complication rate, type of complications, or degree of abdominal pain between the CEUS and US groups (P > 0.05). However, significant differences were observed in the first puncture success rate and the number of sampling (P < 0.05). Importantly, before and after PSM, the CEUS group achieved a higher first-puncture success rate while obtaining a lower number of sampling (P < 0.05). Compared to the US group, the CEUS group demonstrated improved accuracy, sensitivity, specificity, PPV, and NPV of 13.1%, 14.9%, 13.4%, 2.5%, and 38.7%, respectively. Furthermore, the significant difference was observed in the AUC for diagnostic performance between the two groups when compared using DeLong’s test (P = 0.043).
Conclusions
Performing CEUS before percutaneous CNB for pancreatic lesions can help achieve better biopsy results, reduce the number of punctures samples, increase the success rate of biopsies, and avoid the need for repeat biopsies.
Keywords: Contrast-enhanced ultrasound, Core needle biopsy, Ultrasound guide, Pancreatic lesions
Introduction
The pancreas is located behind the peritoneum, surrounded by complex anatomical structures. Among pancreatic lesions, pancreatic cancer exhibits high aggressiveness and mortality rates. Early detection is considered the most effective method for improving survival rates [1, 2]. Making treatment decisions regarding pancreatic lesions involves determining whether the lesions are benign or malignant, which is directly related to prognosis and survival.
Pancreatic biopsy is performed to effectively determine whether the lesions are benign or malignant. Even when imaging and laboratory tests provide evidence of malignancy, a biopsy is necessary to clarify the pathological type and degree of differentiation of pancreatic lesions, thereby determining subsequent treatment methods. Imaging-guided pancreatic biopsy includes computed tomography (CT), magnetic resonance imaging (MRI), and ultrasound (US) guidance. US-guided percutaneous core needle biopsy (CNB) can be used to accurately and safely obtain a histological diagnosis of abdominal lesions. The advantages of US guidance include real-time visualization of the biopsy path and target, clinical practicability, portability, absence of radiation, a relatively short operation time, and low cost [3].
Based on the type of needle used, biopsy methods are further classified into US-guided CNB and fine-needle aspiration (FNA). The success rate of percutaneous US-guided CNB for pancreatic lesions is higher than that of FNA [4]. CNB enables the acquisition of more histological specimens, which can provide clinicians with a more accurate pathological diagnosis. However, pancreatic lesions may exhibit necrosis and severe fibrosis because of continuous tumor growth. Biopsies that reach these areas may yield false negative results, thereby affecting the success and accuracy of the procedure. Contrast-enhanced ultrasound (CEUS) can provide additional useful information, such as a more accurate visualization of microvascular perfusion in the lesion area and the surrounding vascular structure, during pancreatic biopsies, thereby determining the optimal percutaneous biopsy path and ensuring the safety of the procedure [5]. The diagnostic accuracy of CEUS combined with percutaneous FNA for pancreatic lesions is higher than that of conventional US-guided FNA [6]. However, the clinical value of CEUS combined with percutaneous CNB warrants further investigation.
Therefore, using a propensity score-matching (PSM) model, this study aimed to evaluate whether the application of CEUS prior to percutaneous CNB of pancreatic lesions can result in better biopsy outcomes.
Materials and methods
Patients
This retrospective study was approved by the Ethics Committee of our institution (approval number: SCCHEC-02-2024-127), and all patients signed informed consent forms before undergoing CEUS and percutaneous US-CNB.
A total of 336 consecutive patients with solid pancreatic lesions who were initially diagnosed in our hospital between January 2017 and June 2023 were enrolled. The feasibility of percutaneous US-CNB was evaluated in all the patients. The inclusion criteria were as follows: (1) newly discovered pancreatic lesions; (2) pancreatic lesions visible on routine US or CEUS; and (3) patients with no contraindications to percutaneous CNB. The exclusion criteria were as follows: (1) patients with incomplete clinical information or failed follow-up, (2) patients cannot cooperate with the puncture operation, and (3) patients with no safe puncture pathway assessed via US.
Based on these criteria, 277 patients were included in this study. From January 1, 2017 to July 29, 2021, 87 cases with solid pancreatic lesions underwent a routine US assessment prior to CNB. In recent years, CEUS plays an important role in the diagnosis and treatment of pancreatic lesions [7, 8]. With the improvement of percutaneous pancreatic puncture technology and the increasing number of patients in our hospital, from July 30, 2021 to June 30, 2023, 190 cases with solid pancreatic lesions underwent CEUS assessment prior to CNB. The patients were divided into a CEUS (n = 190) and US (n = 87) group based on whether they underwent CEUS prior to CNB. Demographic characteristics, ultrasonic features of the lesions, and clinical data were obtained from the patients’ medical records. A flowchart of patient inclusion is illustrated in Fig. 1.
Fig. 1.
Flow diagram of patients’ inclusion
US and CEUS
The sonographer had over 15 years of experience in CEUS and CNB. Prior to CNB, conventional US was used to assess the size, location, internal echogenicity, and vascular distribution of the pancreatic tumor, and the major vessels surrounding the pancreas. This evaluation determined the availability of a safe needle-biopsy path with concurrent image storage. The pancreatic tumor size was defined as the maximum tumor diameter measured using US. The patients in the CEUS group underwent CEUS after a routine US assessment prior to CNB. CEUS was performed using a Mindray RS90 (Mindray Medical Corporation, Shenzhen, China) equipped with a 3–9 MHz linear probe and 2–5 MHz microconvex array intervention probe, as well as a Siemens Acuson S3000 (Siemens Medical Solutions, Erlangen, Germany) with a 4–9 MHz linear probe and 1–6 MHz convex array probe. SonoVue (Bracco, Spa, Milan, Italy) was used as the ultrasonic contrast agent for CEUS in the enrolled patients. A 2.4-mL SonoVue suspension was administered for the first intravenous injection lasting 2–3 s; 1.0 mL SonoVue was used if a second observation was needed. After injecting the contrast agent, the target lesion was observed continuously for over 3 min, and dynamic images were stored in the ultrasonic instrument. The needle biopsy path for the CNB was evaluated using CEUS. By observing perfusion and contrast enhancement patterns, we assessed the presence of necrotic or severely fibrotic areas (i.e., areas with no contrast agent perfusion) within the tumor. During CNB, avoiding such areas and blood vessels before proceeding with surgery is necessary.
Percutaneous CNB technique
All the patients undergoing CNB were informed of the risks associated with the procedure, including pain, bleeding, and damage to adjacent organs, before the operation. Surgery was performed only after the patient provided informed consent. The patients were required to fast for 8–12 h before surgery, and preoperative blood tests were conducted to assess blood routine parameters, coagulation function, and infectious diseases. Additional tests, such as electrocardiography and chest radiography, were performed when necessary. Preoperative symptomatic and preventive treatments were administered to patients with a tendency for bleeding and poor coagulation function. Contraindications for CNB were as follows: (1) patients who were unable to tolerate the puncture biopsy or cooperate with breathing during the procedure; (2) patients with a significant tendency to bleeding or coagulation disorders; (3) patients with acute pancreatitis or chronic pancreatitis with acute exacerbation; (4) patients with severe cirrhosis and numerous ascites; (5) patients with significant dilation of the pancreatic duct that could not be avoided, as puncture can lead to pancreatic fistula; (6) patients with gastrointestinal obstruction or significant dilation of the intestine; (7) patients with extremely rich blood vessels within or around the tumor, with no safe puncture path. All biopsy procedures were performed in a semi-sterile environment by the same interventional sonographer who performed the preoperative CEUS (primary operator) and another interventional sonographer with over 3 years of experience (assistant).
Using the same ultrasonic instrument employed for the preoperative CEUS as the guiding imaging device, a linear or convex array intervention probe helped guide the images. For CNB, a 17G and 60- or 100-mm coaxial positioning needle (Merit Medical Systems, Inc., Tijuana, Baja California, Mexico) was paired with an 18G and 110- or 150-mm automatic biopsy needle (Merit Medical Systems, Inc., Tijuana, Baja California, Mexico). The cutting length of the biopsy needle was approximately 10–20 mm. At least one tissue sample measuring 10–20 mm in length was required for a successful biopsy; otherwise, the biopsy was considered unsuccessful. The adequacy of biopsy samples was determined via pathological examination.
The patient was placed in a suitable supine or lateral position, and a safe puncture path and puncture point were repeatedly confirmed before the procedure. After routine disinfection and draping, 2% lidocaine was injected at the selected puncture point to induce local anesthesia up to the peritoneal layer. The microconvex array intervention or linear probe was pressed firmly against the abdominal wall, and the shortest possible puncture path was selected for biopsy. The direction and position of the probe were adjusted in real-time to visualize the puncture path clearly.
A coaxially positioned needle was inserted into the peritoneal wall at the selected puncture point, and the coaxial technique was used to establish a subcutaneous tunnel for the biopsy needle, thereby preventing needle deviation and reducing the risk of needle-track seeding. Subsequently, the biopsy needle was inserted along with the coaxially positioned needle, and the patients were instructed to hold their breath during needle insertion. Upon reaching the edge of the target lesion, the trigger was pressed, and the needle was withdrawn quickly, ensuring that the needle tip did not damage the blood vessels deep in the lesion after ejection.
The position of the needle track within the target lesion after biopsy was observed and 2–3 biopsies were performed in different areas (in this study, 1–4 biopsies were performed, depending on the patient’s tolerance and adequacy of the biopsy samples, while ensuring safety). After each biopsy, pressure was applied to the puncture site to stop the bleeding, and the CNB specimens were fixed in a 10% formalin solution for pathological examination.
All the patients who underwent percutaneous CNB underwent comprehensive preoperative assessments using conventional US and CEUS, with most patients adopting an intraperitoneal approach. In cases where direct puncture of the pancreatic lesions was not possible, we used the transhepatic route. If a re-biopsy was required, the patients were re-evaluated after an interval of 5–7 days. Postoperatively, the patients were required to stay in the observation room for 1 h and were discharged only after confirming the absence of active bleeding or other serious complications via US. Routine fasting for > 2 h was required postoperatively.
Final diagnosis
The final diagnosis was confirmed by pathological, clinical, and imaging examinations performed over at least 12 months. If the pathological diagnosis after the percutaneous biopsy or surgery indicated a primary malignant or metastatic pancreatic tumor, the final diagnosis was malignant. Conversely, in patients with a benign pathological diagnosis after the percutaneous biopsy and no change in the size and morphology of the pancreatic lesion during follow-up imaging, the final diagnosis was benign.
Statistical analysis
All the analyses were performed using the SPSS 25.0 statistical analysis software (IBM, Corp., Armonk, NY) and R version 4.4.3 (https://cran.r-project.org/bin/windows/base/). Descriptive statistics were used to assess the frequency distribution of all patients. Categorical variables are presented as frequency (percentage), whereas continuous variables are expressed as mean ± standard deviation. Depending on the data type, the Chi-square test, Fisher’s exact test, Mann–Whitney U test, and independent t-test were used for intergroup comparisons. The 1:1 PSM of nearest neighbor matching methods was used to compare percutaneous biopsy results between the CEUS and US groups with the aim of controlling for potential selection bias. DeLong’s test was used to compare the area under the curve (AUC) of the two groups. All the P values were two-sided, and statistical significance was set at P < 0.05.
Results
Patient demographics before and after PSM
This study included 277 patients with pancreatic lesions who underwent percutaneous biopsy before PSM, with 173 males and 104 females (age: 32–88 years). The baseline patient characteristics are presented in Table 1. Based on whether CEUS was performed before CNB, the patients were divided into the CEUS (190 patients) are US (87 patients) group. A comparison of the baseline clinical and pathological characteristics between the two groups revealed significant baseline differences in tumor size and location. Patients in the CEUS group had larger tumors with diameters > 4 cm (P = 0.047), which were more frequently located in the pancreatic head and tail (P = 0.045). After controlling for these biases using PSM, 70 patients in the CEUS group were compared with 70 patients in the US group, and all patient characteristics and pancreatic lesions remained balanced, SMDs < 0.1 indicated good component balance after matching (Table 1). The PSM details are presented in Fig. 2.
Table 1.
Patient baseline characteristics before and after matching
| Before matching | After matching | |||||||
|---|---|---|---|---|---|---|---|---|
| Characteristics | US group (n = 87) |
CEUS group (n = 190) |
P value | SMDs | US group (n = 70) |
CEUS group (n = 70) |
P value | SMDs |
| Gender, n (%) | ||||||||
| Male | 61 (70.1%) | 112 (58.9%) | 0.075 | -0.227 | 45 (64.3%) | 47 (67.1%) | 0.722 | 0.058 |
| Female | 26 (29.9%) | 78 (41.1%) | 25 (35.7%) | 23 (32.9%) | ||||
| Age (years) | ||||||||
| Range | 33 ~ 80 | 32 ~ 88 | 34 ~ 80 | 40 ~ 86 | ||||
| Mean ± SD | 60.43 ± 10.59 | 62.12 ± 10.73 | 0.221 | 0.158 | 61.46 ± 10.16 | 62.07 ± 9.91 | 0.718 | 0.057 |
| Tumor size (cm) | ||||||||
| Range | 1.7 ~ 10.9 | 1.1 ~ 9.8 | 1.1 ~ 9.8 | 1.7 ~ 9.4 | ||||
| Mean ± SD | 4.78 ± 1.71 | 5.23 ± 1.77 | 0.047 | -0.207 | 4.89 ± 1.67 | 4.74 ± 1.51 | 0.589 | -0.122 |
| ≤ 4 cm | 30 (34.5%) | 49 (25.8%) | 0.137 | 22 (31.4%) | 23 (32.9%) | 0.856 | ||
| >4 cm | 57 (65.5%) | 141 (74.2%) | 48 (68.6%) | 47 (67.1%) | ||||
| Tumor location, n (%) | ||||||||
| Head | 37 (42.5%) | 74 (39.0%) | 0.045 | 0.057 | 28 (40.0%) | 35 (50.0%) | 0.084 | -0.101 |
| Neck | 7 (8.0%) | 13 (6.8%) | 5 (7.1%) | 1 (1.4%) | ||||
| Body | 21 (24.2%) | 26 (13.7%) | 16 (18.6%) | 8 (11.4%) | ||||
| Tail | 22 (25.3%) | 77 (40.5%) | 21 (34.3%) | 26 (37.2%) | ||||
| Final diagnosis, n (%) | ||||||||
| Benign lesion | 11 (12.6%) | 21 (11.1%) | 0.701 | -0.065 | 10 (14.3%) | 6 (8.6%) | 0.288 | 0.037 |
| Malignant lesion | 76 (87.4%) | 169 (88.9%) | 60 (85.7%) | 64 (91.4%) | ||||
CEUS, contrast-enhanced ultrasound; SMDs, standardized mean differences; SD, standard deviation; US, ultrasound
Fig. 2.
Propensity score matching of the 277 patients with pancreatic lesions undergoing CNB. The following two groups were compared after propensity score matching: 70 patients who underwent CEUS before CNB and 70 patients who did not undergo CEUS before CNB. (A) Propensity score matching jitter plot. (B) Propensity score matching histogram. CNB, core needle biopsy; CEUS, contrast-enhanced ultrasound
CNB relevant characteristics before and after matching
All the patients underwent their first CNB for pancreatic lesions in our hospital. Overall, 9 and 10 patients in the CEUS and US group, respectively, had inconclusive pathological results from their initial biopsies and required a second CNB to confirm the pathological type. No patient experienced severe complications, such as pancreatitis, peritonitis, abdominal organ injury, or needle tract seeding, following the puncture. Postoperative mild abdominal pain, moderate abdominal pain with a small amount of peripancreatic bleeding, and fever occurred in 19, 11, and 4 patients, respectively. All the patients recovered after symptomatic treatment. Before and after PSM, no significant differences were observed in the incidence and type of complications or degree of abdominal pain between the two groups (P > 0.05). However, significant differences were observed in the first-puncture success rate and the number of sampling obtained (P < 0.05). Notably, before and after PSM, the CEUS group achieved a higher first-puncture success rate while requiring fewer punctures to obtain samples (P < 0.05; Table 2). CEUS further revealed the blood supply to the pancreatic lesion, helping to identify biopsy paths, avoid puncturing blood vessel areas, and decrease biopsy complications (Fig. 3). CEUS also revealed the necrotic areas in the pancreatic lesions and improved diagnostic accuracy (Fig. 4).
Table 2.
CNB relevant characteristics before and after matching
| Before matching | After matching | |||||
|---|---|---|---|---|---|---|
| Characteristics | US group (n = 87) |
CEUS group (n = 190) |
P value | US group (n = 70) |
CEUS group (n = 70) |
P value |
| First-puncture success rate (%) | 88.51% | 95.26% | 0.039 | 85.71% | 97.14% | 0.031 |
| Number of sampling | ||||||
| 1 | 6 (6.9%) | 4 (2.1%) | 0.013 | 6 (8.6%) | 1 (1.4%) | 0.010 |
| 2 | 23 (26.4%) | 81 (42.6%) | 16 (22.9%) | 30 (42.9%) | ||
| 3 | 57 (65.5%) | 99 (52.1%) | 47 (67.1%) | 35 (50.0%) | ||
| 4 | 1 (1.2%) | 6 (3.2%) | 1 (1.4%) | 4 (5.7%) | ||
| Complication rate (%) | 16.1% | 16.3% | 0.963 | 7.1% | 8.6% | 0.753 |
| Type of complications | ||||||
| Abdominal pain | 9 (10.3%) | 21 (11.1%) | 0.892 | 2 (2.8%) | 3 (4.2%) | 0.946 |
| Minor peri-pancreatic bleeding | 4 (4.6%) | 7 (3.7%) | 2 (2.8%) | 2 (2.8%) | ||
| Fever | 1 (1.2%) | 3 (1.6%) | 1 (1.4%) | 1 (1.4%) | ||
| Degree of abdominal pain | ||||||
| Mild | 5 (5.8%) | 14 (7.4%) | 0.687 | 3 (4.2%) | 5 (7.1%) | 0.580 |
| Moderate | 4 (4.6%) | 7 (3.7%) | 2 (2.8%) | 2 (2.8%) | ||
| Severe | 0 (0%) | 0 (0%) | 0 (0%) | 0 (%) | ||
Fig. 3.
A 55-year-old female patient with a pancreatic mass. (A) Gray-scale US imaging shows a hypoechoic lesion (arrow) in the head of the pancreas with an irregular shape (size 10.6 × 8.0 × 8.5 cm³). (B) Color Doppler flow imaging shows the peripheral and internal vascular distribution of the hypoechoic lesion. (C) CEUS shows rapidly enhanced lesions (arrow) in the arterial phase at 9s. (D) US guide CNB puncture needle (arrow) along the coaxial positioning needle into the pancreatic lesion; three tissue strips were obtained via the puncture. (E) The pathological diagnosis after CNB was Burkitt’s lymphoma (hematoxylin and eosin staining, ×100). CNB, core needle biopsy; CEUS, contrast-enhanced ultrasound; US, ultrasound
Fig. 4.
A 79-year-old female patient with a pancreatic mass. (A) Gray-scale US imaging shows a hypoechoic lesion (arrow) in the tail of the pancreas with an unclear margin (size 4.1 × 3.1 × 3.6 cm³). (B) Color Doppler flow imaging shows the peripheral and internal vascular distribution of the hypoechoic lesion. (C) CEUS shows no enhanced area (arrow) on the surface of the lesion at 38s; CNB should be avoided in this area as much as possible. (D) US guide CNB puncture needle (arrow) along the coaxial positioning needle into the pancreatic lesion; two tissue strips were obtained via the puncture. (E) The pathological diagnosis after CNB was low differentiated adenocarcinoma of colonic origin (hematoxylin and eosin staining, ×100). CNB, core needle biopsy; CEUS, contrast-enhanced ultrasound; US, ultrasound
Final diagnosis of the US and CEUS groups
The final diagnosis for all the patients was made through comprehensive consideration of the pathological and clinical findings. A summary of the pathological subtypes is presented in Table 3. Pancreatic ductal adenocarcinoma, metastatic cancer, and other primary pancreatic malignancies accounted for 88.6% (217/245), 4.9% (12/245), and 6.5% (16/245) of all malignant tumors, respectively. Of the final diagnoses, 88.4% (245/277) of the patients with pancreatic malignancies, after confirmation of the pathology results, underwent multidisciplinary comprehensive treatment, such as surgical treatment (surgical resection), internal medicine treatment (radiotherapy and chemotherapy), and interventional therapy. The remaining 11.6% (32/277) of the patients with benign pancreatic lesions survived during follow-up and were treated via surgery, symptomatic comprehensive treatment, or regular follow-up based on the pathology results. No peritoneal metastasis or needle tract seeding was observed in any patient during the follow-up period. Additionally, no significant difference was observed in the ratio of pancreatic malignancies to benign tumors between the two groups (P = 0.701).
Table 3.
Final diagnosis of the US and CEUS groups
| Diagnosis | Total (n = 277) |
US group (n = 87) |
CEUS group (n = 190) |
|---|---|---|---|
| Benign | 32 | 11 | 21 |
| Chronic pancreatitis | 15 (46.9%) | 5 (45.4%) | 10 (47.6%) |
| NET (G1 or G2) | 8 (25.0%) | 3 (27.3%) | 5 (23.8%) |
| SPN | 3 (9.3%) | 1 (9.1%) | 2 (9.4%) |
| IgG4-associated pancreatitis | 2 (6.3%) | 1 (9.1%) | 1 (4.8%) |
| MCN | 2 (6.3%) | 1 (9.1%) | 1 (4.8%) |
| Heterotopic thyroid tissue | 1 (3.1%) | 0 (0%) | 1 (4.8%) |
| Tuberculosis | 1 (3.1%) | 0 (0%) | 1 (4.8%) |
| Malignant | 245 | 76 | 169 |
| Ductal adenocarcinoma | 217 (88.6%) | 66 (86.9%) | 151 (89.2%) |
| Adenosquamous carcinoma | 7 (3.0%) | 3 (4.0%) | 4 (2.4%) |
| Neuroendocrine carcinoma | 5 (2.0%) | 1 (1.3%) | 4 (2.4%) |
| Lymphoma | 3 (1.2%) | 2 (2.6%) | 1 (0.6%) |
| Liposarcoma | 1 (0.4%) | 0 (0%) | 1 (0.6%) |
| Metastatic lung carcinoma | 5 (2.0%) | 2 (2.6%) | 3 (1.8%) |
| Metastatic colon carcinoma | 3 (1.2%) | 0 (0%) | 3 (1.8%) |
| Metastatic kidney carcinoma | 2 (0.8%) | 1 (1.3%) | 1 (0.6%) |
| Metastatic cervical carcinoma | 2 (0.8%) | 1 (1.3%) | 1 (0.6%) |
MCN, mucinous cystic neoplasms; NET, neuroendocrine tumors; SPN, solid pseudo-papillary neoplasm
Diagnosis performance of the US and CEUS groups
Compared to the US group, the CEUS group exhibited improved accuracy, sensitivity, specificity, positive predictive value (PPV), and negative predictive value (NPV) of 13.1%, 14.9%, 13.4%, 2.5%, and 38.7%, respectively. Furthermore, using DeLong’s test, significant difference was observed in the AUC of the diagnostic performance between the two groups (P = 0.043; Table 4).
Table 4.
Diagnostic performance of the US and CEUS groups
| Group | Accuracy | Sensitivity | Specificity | PPV | NPV | Youden index | AUC (95% CI) |
|---|---|---|---|---|---|---|---|
| US | 0.816 | 0.816 | 0.818 | 0.969 | 0.391 | 0.634 | 0.817 (0.720–0.892) |
| CEUS | 0.947 | 0.965 | 0.952 | 0.994 | 0.778 | 0.917 | 0.958* (0.919–0.982) |
* represents that there is a significant difference existed between the US and CEUS groups
Discussion
This study compared the effectiveness of percutaneous CNB with and without CEUS for pancreatic lesions. Before and after PSM, the CEUS group achieved a higher first-puncture success rate while requiring fewer punctures to obtain samples. Using CEUS prior to percutaneous CNB for pancreatic lesions improved the diagnostic performance, accuracy, sensitivity, specificity, PPV, and NPV.
Image-guided percutaneous biopsy of pancreatic lesions can provide accurate pathological diagnosis, which is crucial for making preoperative treatment decisions for operable patients and selecting the appropriate radiotherapy, chemotherapy, or comprehensive treatment approach for non-operable patients. The accuracy and sensitivity of CT-guided percutaneous CNB for pancreatic lesions is 89.9–100.0% and 88.8–100.0%, respectively [9, 10]. MRI-guided percutaneous CNB for pancreatic lesions has an accuracy of 92.4% and sensitivity of 92.1% [11]. The accuracy and sensitivity of US-guided percutaneous biopsy of pancreatic lesions is 95.2–95.5% and 94.9–95.3%, respectively [4, 12]. In our study, the CEUS group achieved similar accuracy (94.7%) and sensitivity (96.5%) for percutaneous CNB of pancreatic lesions. The lower accuracy and sensitivity in the US group may be due to the relatively small number of patients, and depend on the operator’s proficiency in percutaneous puncture techniques.
The European Federation of Societies for Ultrasound in Medicine and Biology recommends CEUS to enhance the accuracy of percutaneous US-guided pancreatic procedures [13]. When a lesion contains necrotic or severely fibrotic areas, CEUS is crucial to accurately guiding the pancreatic biopsy [6]. CEUS is a more real-time, convenient, radiation-free, and cost-effective imaging modality compared with other modalities. Our study confirmed that CEUS before biopsy can comprehensively determine the biopsy path and accurately locate the lesion boundary and distribution of surrounding vessels. The US-guided technique enables the selection of a skin-to-target tumor path from multiple planes and angles, and ultimately ensures the success of the puncture when combined with coaxial needle technology, probe compression, or patient breath-holding.
We used an 18G needle for puncture and biopsy to obtain sufficient tissue samples for pathological diagnosis. The overall incidence of complications related to puncture was only 12.3%, with no serious complications. Moreover, no significant differences were observed in the occurrence of complications before and after PSM between the two groups. Using CNB for biopsies of pancreatic lesions was superior in acquiring sufficient tissue for pathological diagnoses [4].
CNB preserves the integrity of tissue structures and enables immunohistochemical testing, which is particularly valuable for identifying special types of tumors, such as neuroendocrine neoplasms and lymphomas [14]. Tissue samples obtained using an 18G needle are sufficient for all types of histopathological diagnoses, regardless of whether the lesions are benign or malignant [15]. Minimizing the number of punctures is another crucial factor for successful biopsy [15]. In the present study, CEUS was used to identify necrotic areas and regions of severe fibrosis within lesions that did not show perfusion with contrast agents. By avoiding these areas as puncture targets, we obtained tissue samples while effectively reducing the number of punctures, thereby ensuring high success and low complication rates.
Compared with conventional US-CNB, CEUS-CNB incurs additional costs for contrast agents and may increase the puncture operation time. However, we believe that CEUS-CNB has a greater clinical value for pancreatic lesions owing to the higher diagnostic performance, biopsy accuracy and first-puncture success rate. We recommend initial US and CEUS for pancreatic lesions needing pathological typing, to assess whether a safe puncture path exists for percutaneous biopsy. If unsuitable, other imaging-guided methods should be considered.
Our study had some limitations. First, the sample size was derived from a single center, and the percutaneous CNB technique for pancreatic lesions requires radiologists with extensive experience in US intervention, which may have affected the generalizability of our findings. Second, as a retrospective study, there remains a potential for selection bias despite conducting a PSM analysis. Future studies with larger sample sizes, multicenter designs, and more comprehensive data collection are needed to overcome these limitations and provide more reliable evidence.
Conclusions
CEUS before biopsy can comprehensively determine the biopsy path and accurately locate the lesion boundary and distribution of surrounding vessels. Performing CEUS before percutaneous CNB for pancreatic lesions can help achieve better biopsy results, reduce the number of punctures required to obtain samples, increase the success rate of biopsies, and avoid the need for repeat biopsies.
Acknowledgements
We would like to thank Editage (www.editage.cn) for English language editing.
Abbreviations
- AUC
Area Under the Curve
- CEUS
Contrast-Enhanced Ultrasound
- CNB
Core Needle Biopsy
- CT
Computed Tomography
- FNA
Fine-Needle Aspiration
- MRI
Magnetic Resonance Imaging
- NPV
Negative Predictive Value
- PSM
Propensity Score Matching
- PPV
Positive Predictive Value
- US
Ultrasound
Author contributions
Q.D., X.W. and T.S. participated in the design of the study, data collection and paper writing. Y.T., L.H. and L.C. and participated in the design of the study and manuscript editing. Q.D., Z.W., X.W. and T.S. participated in the design of the study and data collection. Q.D., Y.T. and X.W. participated in the design of the study and helped to revise the manuscript. All authors read and approved the final manuscript.
Funding
This research did not receive any specific grant from any funding agency in the public, commercial or not-for-profit sector.
Data availability
The datasets generated or analyzed during the study are available from the corresponding author on reasonable request.
Declarations
Ethics approval and consent to participate
This study was approved by The Ethics Committee of the Sichuan Cancer Institute & Hospital (approval number: SCCHEC-02-2024-127). This study was performed in accordance with the Declaration of Helsinki. Written informed consent was obtained from all patients enrolled in this study.
Consent to participate
Written informed consent was obtained from individual or guardian participants.
Consent for publication
Not applicable.
Competing interests
The authors declare no competing interests.
Footnotes
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Tiefeng Shi and Xiaobo Wu contributed equally to this work.
Contributor Information
Tiefeng Shi, Email: shitiefeng1970@163.com.
Xiaobo Wu, Email: 520527966@qq.com.
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Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Data Availability Statement
The datasets generated or analyzed during the study are available from the corresponding author on reasonable request.




