INTRODUCTION — Exocrine pancreatic cancer is a common cause of cancer-related death in the United States and is second only to colorectal cancer as a cause of digestive cancer-related death [1,2]. Surgical resection offers the only potential cure, but because of the late presentation of the disease, only 10 to 15 percent of patients are candidates for pancreatectomy, and five-year survival rates are very low. (See "Epidemiology and nonfamilial risk factors for exocrine pancreatic cancer" and "Overview of surgery in the treatment of exocrine pancreatic cancer and prognosis".)
The main obstacles to potentially curative resection are the presence of distant metastases and/or invasion of nearby major vascular structures. A variety of studies are available for preoperative diagnosis and staging of pancreatic cancer, including:
●Transabdominal ultrasound
●Abdominal computed tomography
●Magnetic resonance imaging
●Endoscopic retrograde cholangiopancreatography
●Positron emission tomography
●Endoscopic ultrasonography
●Angiography
This topic will review the role of endoscopic ultrasound in the staging of pancreatic cancer. The general approach to the diagnosis and staging of pancreatic cancer is discussed separately. (See "Clinical manifestations, diagnosis, and staging of exocrine pancreatic cancer".)
TECHNIQUE — The technical aspects of performing endoscopic ultrasound (EUS) and EUS-guided fine-needle aspiration or biopsy are presented elsewhere. (See "Endoscopic ultrasound-guided fine needle aspiration in the gastrointestinal tract" and "Endoscopic ultrasound-guided fine needle biopsy in the gastrointestinal tract".)
STAGING — Staging patients with pancreatic cancer includes determining the tumor-node-metastasis (TNM) stage (table 1), as well as evaluating for vascular invasion [3]. (See "Clinical manifestations, diagnosis, and staging of exocrine pancreatic cancer", section on 'Imaging studies'.)
Multiple imaging modalities, including endoscopic ultrasound (EUS), are available for staging pancreatic cancer. EUS is typically used to further evaluate patients with nonmetastatic disease that appears resectable on initial imaging (eg, computed tomography or magnetic resonance imaging) [4]. (See 'Clinical algorithm' below.)
Goal of staging — The goal of preoperative staging is to identify patients who might benefit from surgery, while avoiding surgery in patients with locally advanced or metastatic disease. However, even with efforts to establish resectability preoperatively, many patients have unresectable tumors at surgery. (See "Clinical manifestations, diagnosis, and staging of exocrine pancreatic cancer".)
TNM staging — Pancreatic cancer is staged using the tumor-node-metastasis (TNM) system, the most recent version of which is outlined in the table (table 1). EUS is useful for tumor and node staging, while alternative imaging modalities, such as computed tomography (CT) or magnetic resonance imaging, are required for metastasis staging. (See "Clinical manifestations, diagnosis, and staging of exocrine pancreatic cancer", section on 'Staging system and the staging workup'.)
In general, EUS is more accurate than CT for T-staging of smaller tumors, whereas CT is more accurate than EUS for larger tumors [5]. EUS appears to be as accurate as helical CT and multidetector row CT for N-staging [6].
Evaluation of vascular invasion — The presence or absence of vascular invasion is a major determinant of tumor resectability. However, vascular invasion does not automatically preclude resection since some vessels involved with the tumor can be resected and reconstructed. Thus, it is important to know whether vascular invasion is present and, if it is, to determine the specific anatomic location and the degree of vascular invasion.
Vascular invasion is probable if any of the following is present [7]:
●Peripancreatic venous collaterals in an area of a mass that obliterates the normal anatomic location of a major portal confluence vessel
●Tumor within the vessel lumen
●Abnormal vessel contour or irregular wall with loss of the vessel-parenchymal sonographic interface
ACCURACY OF EUS — The reported accuracy of endoscopic ultrasound (EUS) for tumor-node-metastasis (TNM) staging and for determining vascular invasion is highly variable among studies [8]. Some studies show superiority to other imaging modalities, while other studies show equivalent or even inferior results for EUS [9]. (See 'Clinical algorithm' below and "Clinical manifestations, diagnosis, and staging of exocrine pancreatic cancer", section on 'Imaging studies'.)
Several factors, such as the experience of the endosonographer and the endosonographer's knowledge of prior diagnostic imaging studies [10], may influence the staging accuracy of EUS. The endosonographer should have performed at least 100 EUS examinations for pancreatic tumor staging [11,12].
The type of instrument used does not appear to influence staging accuracy. Both radial and linear array EUS instruments perform equally well, although the latter has the advantage of permitting fine-needle aspiration (FNA) biopsies to be obtained [13]. (See 'EUS-FNA' below.)
TNM stage — The reported accuracy of EUS for T-staging is highly variable, ranging from 63 to 94 percent, with reported accuracies for N-staging ranging from 44 to 82 percent [4,10,12,14-21]. Comparing studies for T-staging is difficult because of changes in T-staging criteria over time. For example, two studies showed an accuracy of 63 and 67 percent for T-staging and 67 and 44 percent for N-staging [20,21]; however, these studies were based on an earlier version of the TNM staging classification. (See "Clinical manifestations, diagnosis, and staging of exocrine pancreatic cancer", section on 'Staging system and the staging workup' and 'Cost-effectiveness' below.)
Vascular invasion — The reported sensitivity of EUS for detecting vascular invasion has varied widely, with estimates ranging from 50 to 100 percent [22]. A meta-analysis of 29 studies showed that EUS had high specificity (90 percent) but only moderate sensitivity (73 percent) for detecting vascular invasion [22].
Analyses have also shown that both sensitivity and specificity have decreased over time [22]. When comparing the time period of 1988 to 1994 with the period of 2000 to 2005, the pooled sensitivity decreased from 90 to 65 percent, and the pooled specificity decreased from 96 to 86 percent. The authors suggest that the decreasing sensitivity seen over time may reflect smaller numbers of patients in earlier studies.
EUS may not be as accurate in excluding vascular invasion in patients with small pancreatic tumors [22]. However, EUS is superior to other imaging modalities, such as CT and transabdominal ultrasound, for detecting vascular invasion in tumors that are smaller than 3 cm (image 1) [23,24].
The accuracy of EUS also varies with the vessel being examined. The accuracy for detecting invasion into the superior mesenteric artery and vein is lower than that for detecting portal or splenic vein invasion [10,11,25].
COMPARISON OF EUS WITH OTHER IMAGING TECHNIQUES — Studies have compared endoscopic ultrasound (EUS) with helical computed tomography (CT), multidetector row CT (MDR-CT), magnetic resonance imaging (MRI), and angiography for initial diagnosis and/or staging of pancreatic cancer [9]. However, direct comparison of the data can be difficult because of differences in inclusion criteria and reference standards. The imaging modalities chosen to stage patients with pancreatic cancer should take into account the studies' accuracy as well as local expertise.
Helical CT — Multiple studies have compared the accuracy of EUS with helical CT for the evaluation of pancreatic cancer resectability [6,20,21,26-32]. However, the studies are heterogeneous, and most had methodologic flaws.
These limitations were highlighted in a systematic review that examined 11 studies with 678 patients [6]. Only three studies met all but one of the quality criteria. The most important and frequent study limitations were lack of a consecutive series of patients and biased patient selection for surgery that potentially affected validity. The older studies included in that review suggested that EUS was superior to CT for staging and determining vascular invasion. However, the more recent studies found that helical CT was more accurate than EUS for T-staging (73 versus 63 percent) and was equivalent for N-staging (62 to 63 percent versus 65 to 69 percent). EUS and CT were also equivalent with regard to detecting vascular invasion. More prospective studies are needed before definitive conclusions can be made.
Multidetector row CT — CT scanners with multiple rows of detectors permit imaging of larger volumes of tissue, while acquiring both arterial and venous phases in shorter periods of time [20,33]. MDR-CT has improved the evaluation of the main pancreatic duct and the detection of small tumors [34].
Only a few studies comparing EUS with MDR-CT for detecting and staging pancreatic cancer are available. In a report of 80 patients who underwent EUS for pancreatic cancer, EUS was superior to MDR-CT for tumor detection (sensitivity 98 versus 86 percent) and primary T-staging (accuracy 67 versus 41 percent), but similar for nodal staging (accuracy 44 versus 47 percent) [21]. Fifty-three patients underwent surgery and 25 were found to have resectable tumors. EUS and MDR-CT correctly identified 88 and 92 percent of the resectable tumors. Of the 28 surgical patients with unresectable tumors, EUS and MDR-CT correctly identified the tumors as being unresectable in 68 and 64 percent.
Angiography — A number of studies have compared the accuracy of EUS and angiography for determining vascular invasion [10,20,25,27,35]. Although the results vary, EUS appears to be as accurate or more accurate for determining vascular invasion, except for tumors that invade the superior mesenteric vein. The following examples illustrate these points:
●One study included 45 patients with pancreatic cancer [25]. Several EUS criteria for vascular invasion were studied, the most accurate of which was the presence of an irregular venous wall (accuracy 87 percent). However, the sensitivity of wall irregularity for detecting vascular invasion was only 47 percent, due in large part to difficulty in detecting invasion of the superior mesenteric vein (sensitivity of 17 percent). In 28 patients who underwent surgical exploration, negative resection margins were attained in 86 percent when both tests were used preoperatively, 78 percent when EUS was used without angiography, and 60 percent when only angiography was used.
●Higher sensitivities were noted in a report of 21 patients with pancreatic cancer who underwent EUS and angiography prior to an attempt at curative resection [35]. EUS was significantly more sensitive than angiography for detecting vascular invasion (86 versus 21 percent) with equivalent specificity (71 percent for both).
Magnetic resonance imaging — Studies comparing EUS with MRI suggest that EUS may be more sensitive for detecting small tumors, while providing complementary information regarding resectability [17,20,36,37].
A retrospective study focused on 63 patients with pancreatic cancer who underwent both examinations, using surgical results as the gold standard [36]. The tumor was resectable in 36 patients (57 percent). The sensitivities of EUS and MRI for determining resectability were 61 and 73 percent, respectively. EUS and MRI both predicted resectability in 18 patients, of whom 16 (89 percent) were found to be resectable at the time of surgery. Both studies predicted unresectability in 17 patients, of whom 13 (76 percent) were unresectable at the time of surgery.
In a prospective study of 48 patients who were staged with EUS and MRI prior to surgery, the correlation between EUS and MRI was fair (kappa 0.42), with agreement in the patient's staging seen in 74 percent [38]. EUS understaged 13 patients (27 percent), whereas MRI understaged 12 (25 percent). Only one patient was overstaged by EUS, and none were overstaged by MRI. MRI was more likely to report metastatic disease or arterial involvement.
PET scanning — Positron emission tomography (PET) scanning has been studied in the evaluation of patients with a variety of malignancies, including pancreatic cancer. PET scanning has a high sensitivity (approximately 90 percent) for detecting pancreatic cancer, but only moderate specificity (approximately 70 percent) since benign inflammatory lesions can mimic cancer [39,40]. Another pitfall of PET is that it provides limited anatomic information, which can be overcome by combining it with CT.
The role of PET scanning for the staging of pancreatic cancer requires further investigation. (See "Clinical manifestations, diagnosis, and staging of exocrine pancreatic cancer", section on 'Positron emission tomography scanning'.)
EUS-FNA — Endoscopic ultrasound-guided fine-needle aspiration (EUS-FNA) may help in the diagnosis and staging of pancreatic cancer in multiple ways. (See "Endoscopic ultrasound-guided fine needle aspiration in the gastrointestinal tract".)
EUS-FNA can be used to:
●Biopsy lesions that are too small to be characterized by computed tomography (CT) or magnetic resonance imaging (MRI) [41]
●Biopsy lesions that are too encased by surrounding vascular structures to permit safe percutaneous biopsy [41]
●Demonstrate malignant invasion of lymph nodes located in the celiac, para-aortic, retroduodenopancreatic, or superior mesenteric regions [42]
●Biopsy suspected small metastases in the left lobe of the liver [43]
●Diagnose carcinomatosis through sampling of ascitic fluid [44]
Indications — The indications for EUS-FNA in patients with pancreatic cancer are controversial. It is generally agreed that histologic confirmation is helpful for planning chemotherapy or radiotherapy in patients with distant metastases who are poor surgical candidates or have advanced locoregional disease [4]. (See "Initial systemic chemotherapy for metastatic exocrine pancreatic cancer" and "Initial chemotherapy and radiation for nonmetastatic, locally advanced, unresectable and borderline resectable, exocrine pancreatic cancer".)
The role of EUS-guided FNA is more controversial in patients who are good surgical candidates with pancreatic cancer that appears to be resectable on other imaging studies. The traditional approach in such patients has been surgery. (See "Clinical manifestations, diagnosis, and staging of exocrine pancreatic cancer", section on 'Diagnostic algorithm and need for preoperative biopsy'.)
In such patients, indications for EUS-FNA currently include [4,26,45,46]:
●Ruling out other types of malignancy involving the pancreas that can mimic adenocarcinoma (eg, lymphoma and small cell carcinoma, metastatic disease, and gastrointestinal neuroendocrine tumors), as well as non-malignant processes such as autoimmune or chronic pancreatitis.
●Assisting with surgical planning (eg, a more limited resection may be possible in patients with neuroendocrine tumors).
●Confirming the diagnosis in patients who want verification prior to surgery. However, as noted in the next section, a negative result does not exclude malignancy.
Accuracy of EUS-FNA — EUS-FNA is technically successful in 90 to 95 percent of procedures, with high sensitivity and specificity [4]. A meta-analysis of 15 studies with 1860 patients found that overall, the sensitivity of EUS-FNA for pancreatic cancer was 92 percent, and the specificity was 96 percent [47]. In a second meta-analysis that included 41 studies with 4766 patients, the pooled sensitivity of EUS-FNA for diagnosing the correct etiology for a solid pancreatic mass was 89 percent, with a specificity of 96 percent [48].
The accuracy, which is defined as the proportion of all test results (both positive and negative) that are correct, appears to be lower in the setting of chronic pancreatitis (74 versus 91 percent in one report) [49], particularly in patients with obstructive jaundice [50].
The benefits of EUS-guided FNA are illustrated by a study of 559 patients undergoing EUS-guided FNA for evaluation of pancreatic masses [51]. In that study, when using strict cytologic criteria, the sensitivity for EUS-guided FNA diagnosing pancreatic adenocarcinoma was 77 percent, with a specificity of 99 percent. When patients with atypical or suspicious cytologies were reclassified as positive for malignancy, the sensitivity increased to 93 percent, without a change in the specificity.
The accuracy of EUS-FNA can improve with additional FNA passes and onsite histologic interpretation [52,53]. In one report, the presence of a cytopathologist in attendance for all aspiration procedures was associated with a high degree of accuracy (95 percent) in diagnosing pancreatic cancer [52]. The absence of a cytopathologist during the EUS-FNA procedure required an average of at least five to six passes from the pancreatic mass to ensure adequate cellularity. In another study, there was a high yield from only two FNA passes when the samples were examined both by histology and cytology [54]. In that study, cytopathologists were not onsite during the procedure.
The size of the needle used for FNA may also be important. In a meta-analysis of eight studies with 1292 patients, the sensitivity of FNA using a 25-gauge needle was higher than that for a 22-gauge needle (1 versus 0.85) with similar specificity (0.97 versus 0.93) [55].
EUS-FNA versus percutaneous image-guided FNA — There are few studies comparing EUS-FNA to alternative sampling techniques such as ERCP, CT-guided FNA/biopsy, or transabdominal ultrasound (US)-guided FNA/biopsy [56-60]. A prospective, randomized crossover trial comparing EUS-FNA with transabdominal US/CT-guided FNA in the diagnosis of pancreatic cancer found no statistical difference between percutaneous and EUS-guided approaches [56]. Although both approaches were most accurate when the average lesion was at least 3 cm in diameter, EUS-FNA was more useful when the US/CT examination was unable to discern small, discrete lesions.
In addition to improved diagnosis of small lesions, EUS-FNA compared with US/CT-guided FNA is associated with reductions in the risk of needle-tract seeding [61], the risk of peritoneal carcinomatosis [62], and cost [63]. (See 'Cost-effectiveness' below.)
Molecular genetic analysis — The addition of molecular genetic analysis (eg, assay for K-ras or p53 gene mutations by RT-PCR or restriction length polymorphisms, promoter methylation of tumor suppressor genes, differential protein expression [proteomics]) to cytologic examination may improve the sensitivity of EUS-FNA for diagnosing pancreatic cancer, especially in patients with small primary tumors [64-71].
In a study with 394 patients with pancreatic masses, K-ras mutations were present in 266 of 307 patients (87 percent) with pancreatic ductal adenocarcinoma and in 3 of 87 patients (3 percent) with non-pancreatic ductal adenocarcinoma [70]. When the results of the K-ras mutation analysis were combined with cytohistopathologic results, the sensitivity for detecting pancreatic ductal adenocarcinoma was 93 percent, and the specificity was 100 percent. However, others report a lower sensitivity (38 percent) of K-ras mutations for the detection of pancreatic cancer [69]. At present, molecular analysis of pancreatic aspirate is not a routine component of the diagnostic evaluation for pancreatic masses.
EUS WITH CORE-NEEDLE BIOPSY — The role of EUS-guided core-needle (trucut) biopsy in the evaluation of pancreatic masses is discussed separately. (See "Endoscopic ultrasound-guided fine needle biopsy in the gastrointestinal tract".)
COST-EFFECTIVENESS — Several analyses of the costs related to the diagnosis and staging of pancreatic cancer have involved strategies using endoscopic ultrasound (EUS) [41,72-75]. Taken together, they suggest that EUS combined with EUS-guided fine-needle aspiration (EUS-FNA) may be a cost-effective strategy for the evaluation of patients suspected of having pancreatic cancer. However, these studies predated the 2017 revision of the TNM staging classification that included changes to the definition of T stage and N stage (table 1). For example, celiac nodal involvement is not regarded as unresectable disease, particularly for tumors located in the head of pancreas; thus, such patients would not necessarily have a change in management. Further studies are needed that use the 2017 TMN classification system in the context of available treatment strategies.
CLINICAL ALGORITHM — An approach to the evaluation of patients with suspected pancreatic cancer is shown in the algorithm (algorithm 1).
SOCIETY GUIDELINE LINKS — Links to society and government-sponsored guidelines from selected countries and regions around the world are provided separately. (See "Society guideline links: Pancreatic cancer".)
SUMMARY AND RECOMMENDATIONS
●Staging patients with pancreatic cancer includes evaluating for tumor-node-metastasis (TNM) stage and determining if vascular invasion is present. (See "Clinical manifestations, diagnosis, and staging of exocrine pancreatic cancer".)
●The goals of preoperative staging are to identify patients who might benefit from surgery and to avoid surgery in patients who have locally advanced or metastatic disease.
●A variety of studies, including endoscopic ultrasound (EUS) and computed tomography, are available for preoperative diagnosis and staging of pancreatic cancer. The imaging modalities chosen should take into account the studies' accuracy as well as local expertise. (See "Clinical manifestations, diagnosis, and staging of exocrine pancreatic cancer".)
●The reported accuracy of EUS for TNM staging and for determining vascular invasion is highly variable. (See 'Accuracy of EUS' above and 'Clinical algorithm' above.)
●Experience of the endosonographer may improve accuracy. We suggest that the endosonographer should have performed at least 100 EUS examinations for pancreatic tumor staging. (See 'Accuracy of EUS' above.)
●The indications for EUS-guided fine-needle aspiration (EUS-FNA) in patients with pancreatic cancer are controversial (see 'EUS-FNA' above). EUS-FNA can be used to:
•Help plan chemotherapy or radiotherapy in patients with distant metastases who are poor surgical candidates or have advanced locoregional disease.
•Rule out other types of malignancy involving the pancreas that can mimic adenocarcinoma, as well as non-malignant processes such as autoimmune or chronic pancreatitis.
•Assist with surgical planning.
•Verify the diagnosis of pancreatic cancer prior to surgery for patients who desire confirmation.
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