Staging Of Pancreatic Masses - The Role Of EUS and Laparoscopy

Introduction

Historically, the accepted median survival of patients with pancreatic carcinoma not treated with chemotherapy or radiotherapy is 11 mo for resected tumors, and 6 mo for unresectable disease. At diagnosis, less than 5% of patients are determined to have resectable lesions: less than 10% of resected patients survive 5 years with a standard therapy. Non-operative palliation is safer, less invasive, and equally effective to relieve jaundice.

The recent improvements in both surgical and nonsurgical treatment for pancreatic carcinoma appear to hold great promise for improving this prognosis. Mortality rates for resection of pancreatic carcinoma including a pancreatoduodenectomy (Whipple operation) have improved to as low as 2-3%. Reports have shown that using improved preoperative staging strategies can decrease the rate of laparotomy without resection.

Pancreatic carcinoma that is unresectable due to local invasion of blood vessels or spread to regional lymph nodes (Stage II/III) has been shown to respond to combined chemotherapy and radiotherapy. Median survival of this Stage II/III group given chemotherapy combined with radiotherapy alone matches the survival of a contemporary group who had resection of less advanced T1 tumors without using chemoradiotherapy. The complications of modern chemoradiotherapy appear to be less than those of the earlier conventional treatments.

Because of the difficulty in obtaining accurate imaging of the pancreas with other methods, EUS may have its greatest impact in the evaluation of the pancreas. Studies show that EUS is more accurate than any other test including ultrasound, CT, MRI, ERCP, and angiography for detection and staging of pancreatic tumors. EUS is also more accurate than CT or other tests for predicting resectability of a pancreatic mass (Table 1). The high resolution images of EUS make it possible to visualize very small lesions, ductal abnormalities, and calcifications not seen with other methods. The accuracy of T staging is consistently good for both pancreatic and ampullary neoplasms (Table 2). T stage also correlates to presence of lymph nodes (Table 3), and survival (Table 4).

The high accuracy of real time EUS of the pancreas is primarily due to both its unsurpassed resolution of the parenchyma of the pancreas and also its capability of evaluating and integrating, on the same exam, mucosal, vascular, ductal and parenchymal abnormalities caused by disease. To obtain information about these four types of abnormalities, four separate tests would otherwise be required: 1. endoscopy for mucosa, 2. venogram or arteriogram for veins and arteries, 3. ERCP for the pancreatic and bile ducts, 4. CT scan or standard sonography for the parenchyma and surrounding lymph nodes.

Indications of EUS of the pancreas now include: 1. staging potentially resectable tumors; 2. detection of endocrine tumors; 3. evaluation of equivocal abnormalities in the pancreas present on other studies. EUS has clearly emerged as the most accurate single test for imaging pancreatic disease.

Making the diagnoses of pancreatic carcinoma in its early stages is very challenging, but this is precisely when it must be made. In patients that do not present with obstructive jaundice, particularly when symptoms are nonspecific such as pain and/or weight loss of unclear etiology, diagnosis can often be difficult to establish. The different conventional imaging modalities such as transcutaneous ultrasonography, CT, ERCP, magnetic resonance, and angiography often will miss pancreatic tumors that are less than 3 cm, especially when chronic pancreatitis is found. The diagnoses of pancreatic carcinoma based on a standard workup including clinical history, physical examination and liver function tests (LFT) often relies on many of these imaging studies, but frequently they will not establish any diagnosis. A mass may not be seen, or the mass can be obscured by pancreatitis. There is no evidence of vessel invasion, biopsies are negative, ERCP findings are not specific. Is laparotomy the next step? The answer is often no. Patients are usually followed with various repeat imaging studies and blood tests at specified intervals searching for a change in a test that indicates a high suspicion of malignancy. Frequently, this finding is one of distant metastasis. Biopsy or laparotomy frequently diagnoses a neoplasm when progression has been significant. There is a low probability of having pancreatobiliary cancer especially with LFT's that are not characteristic of biliary obstruction.

On the other hand, patients with jaundice without evidence of stones or fever have a high probability of having pancreatobiliary cancer especially with liver function tests (LFT's) characteristic of biliary obstruction. However, frequently no diagnosis is established. Full evaluation with more standard imaging tests is not helpful. Is laparotomy the next step? The answer is often yes, because frequently a tumor is found when obstructive jaundice is present. A pancreatoduodenectomy Whipple resection can be performed.

Endoscopic ultrasonography (EUS) has been shown in many studies to provide highly detailed images of the pancreas and associated tumors. There is a significant learning curve in performing optimal EUS of the pancreas. In a recent report on 192 with neoplastic disease, accuracy was 93%, sensitivity 94%, and specificity 92% for EUS for diagnosis of neoplastic disease. This was higher than the values of 83%, 85%, and 80%, respectively, which were reported for initial experience with the first 60 patients. Necrotic pancreatitis simulating a tumor even at laparotomy was found in 9% of patients undergoing resection and is still an important cause of a false positive evaluation.. Of note, EUS found metastasis in 2/3 of patients eventually proven to have metastatic disease who had preoperative CT that was negative for metastatic disease. In 50% of the M1 patients where EUS did not find metastasis, EUS found significant unresectable tumor outside the pancreas. Of those patients with T3 stage on EUS who nevertheless underwent laparotomy, resection could not be performed in 64%. In the 36% in which "resection" was carried out, all neoplasms had to be shaved off a major vessel, or the patients required vessel resection or a vessel graft, except in 3 cases which had necrotic pancreatitis at resection. Tumor resection or Whipple was performed in 79% of those with T1 tumors and in 72% with T2 tumors.

Of the 192 patients with neoplastic disease, based on EUS 57% were predicted not to benefit from attempted resection. On initial CT, almost all of the patients evaluated with EUS in this study had what appeared to be resectable disease. Based on EUS findings alone, resection of disease could be performed in 79% of those with T1 tumors, in 72% with T2 tumors, but in only 36% with T3 tumors. Resection of those patients staged as T3 with EUS was usually more complex, requiring shaving of tumor off a major vessel or resecting or grafting of a vessel. Two of the three T3 tumors found in surgical patients staged with EUS as T1 or T2, had extensive spread to lymph nodes which could have been confirmed with laparoscopy.

For tissue diagnosis, EUS fine needle aspiration (FNA) has been shown by Vilmann et al., to have an accuracy of 83% with a negative predictive value of 76%. This accuracy is a significant improvement over CT or standard ultrasound guided FNA, for which negative predictive value is less than 50% especially for tumors less than 3cm.

Using preoperative evaluation with selective use of EUS, angiography and laparoscopy, Cooperman performed 66 Whipple operations in over two and one-half years. Resectability rate was 88%. Fewer operative surprises contributed to a very low (1.6%) mortality rate; there was one non-procedure related myocardial infarction death. Two patients required reoperation for operative complications. To evaluate resectability, EUS was generally performed as the initial test after CT, prior to angiography. In selected cases, laparoscopy was performed just prior to laparotomy for resection. With this algorithm, laparoscopy detected less than 5% with metastatic disease that was not detected by any other tests, including EUS. Cooperman concluded that "since pancreatic cancer is virtually incurable, continued emphasis on surgery as the sole therapy is fruitless. Surgery is rarely curative, and is unnecessary for palliation. Resectability rates and survival rates can be improved with adjuvant chemotherapy, possibly combined with radiation therapy".

Warshaw and associates reported on a staging protocol of sequential evaluation with dynamic CT, laparoscopy and angiography with special attention to venous phase; 78% of their patients predicted to have resectable cancer in the head of the pancreas were actually resectable at laparotomy. When they added EUS after laparoscopy, resectability rate increased to 86%. Comparing these findings to Cooperman's data, EUS appears to prevent unnecessary laparotomy in an additional 10%. If EUS is used as the initial test to evaluate resectability, a significant number of patients may avoid angiography as well as laparoscopy. Most cases that were shown to be unresectable on laparoscopy or angiography had disease that on EUS would have been predicted unresectable. Thus, EUS alone will find most cases with unresectable disease, as it is the most accurate single test for this purpose. For staging, 3D-CT scan can confirm EUS findings when needed. For tissue diagnosis, EUS-FNA can be used when needed.

Ultrasonography can now also be performed during laparoscopy. Using laparoscopic ultrasonography (LUS), Conlon has been able to improve resection rates to above 90%. At Memorial Sloan Kettering (MSK), positive predictive value for resection rates based on CT alone are 58%. Adding laparoscopy improves resection rates to 77%; adding LUS improves resection rates to 91%. Laparoscopy has reduced costs by about 25%, compared to the approach at MSK of performing a laparotomy based on CT and other imaging test findings.

The number of laparotomies avoided by using effective preoperative evaluations, with and even without EUS, is dramatic when one compares the results of Cooperman, Warshaw and Conlon to traditional surgical series, which report only a 10 to 25% resectability rate of those patients undergoing attempted resection, with a mean operative mortality rate of 15-26%. A thorough preoperative evaluation including a careful selection of CT, extracorporeal US, ERCP with stents of the bile ducts, EUS, angiography, laparoscopy, and LUS will determine patients most likely to have a resectable pancreatic tumor. The order in which these tests should be performed, and how many need to be performed to be most cost effective, has yet to be determined. Although CT can visualize the pancreas in over 90% of cases, a tumor must be at least 2 to 3cm for probable detection. A mass may not even be detectable by CT in about 20% of patients preoperatively assumed to have resectable carcinoma before EUS assessment is performed.

Assessment of resectability with CT is even less reliable than either simple detection of a tumor. CT accuracy for resectability is less than 50% for small tumors, even with thin section CT. Comparative data are available for spiral CT in 3 studies confirming that EUS is unsurpassed in determining resectability, with an accuracy of 75 to 97%. Determining vascular involvement of pancreatic tumors with EUS is at least as accurate as with angiography. Accuracy of angiography alone in predicting resectability is 54 to 80%.

Most patients with pancreatic tumors are evaluated by combinations of imaging tests rather than a single test. Only 2 studies prospectively compare EUS accuracy to the combined accuracy of CT scan plus ERCP in differentiating malignant from inflammatory pancreatobiliary tumors. One study showed that EUS was superior, and the other study showed that CT scan plus ERCP was better. The difference between the two studies was the mean tumor size of the population studied. Rosch et al. reported on a group of patients with a mean tumor size of 4.5cm (range = 2 to 20cm) and found CT plus ERCP superior to EUS. But they also pointed out that, similar to Yasuda et al., they found EUS superior to CT or ERCP for tumors measuring less than 3cm. Snady et al. reported on a group of patients with a mean tumor size less than 3cm (range= 1 to 5cm) and found EUS was superior. Combined data from the two studies supports the concept that the larger a tumor is, the less the difference between the accuracy of EUS and of CT scan plus ERCP will be. For smaller, potentially resectable tumors, the greater the difference will be in favor of EUS.

Performing EUS early in the evaluation of patients with tumors that appear to be localized and less than 5cm on transcutaneous ultrasonography or CT is likely to be effective in terms of clinical utility (Figure 1). For patients with small pancreatic tumors, resection is generally considered both to be the best palliation and to offer the best chance of improved survival. Correctly identifying the patient with resectable pancreatic carcinoma and no metastatic disease or vessel involvement would spare many others a major operation. Reviewing the data from various studies shows that EUS, when used in the appropriate clinical setting, will significantly change the management in about 1/3 of patients, either by making a diagnosis or by changing an incorrect diagnosis or tumor stage. If EUS shows that the tumor is resectable, then laparoscopy to exclude small metastatic foci, generally not seen on CT scan in up to 40%, may prove beneficial prior to attempted resection, depending on the characteristics of the patient group being evaluated. In certain cases, LUS, 3D-CT, or angiography may be used to confirm EUS findings. EUS should most effectively influence management if pancreatic tumor size on initial US or CT without contrast is the primary factor determining the diagnostic and treatment protocol.

CT has eliminated invasive evaluation of advanced tumors. EUS is unlikely to provide additional information for patients with large tumors because the EUS probe can not always be brought close enough to a large lesion to bring its margins into optimum focus. In these cases, diagnosis with fine needle biopsy, followed by palliative bypass of the biliary obstruction, preferably with stents if local expertise permits, or with surgical bypass, is straightforward. Tumors greater than 5cm are resectable in less than 10%. Patients with large tumors can be treated most effectively with chemoradiotherapy. The one exception to not using surgery as the initial treatment is the unusual patient with pancreatic cancer who presents with duodenal or gastric outlet obstruction without obvious metastatic disease. This event is rare (2 in 600 cases) since obstruction tends to be such a late symptom of pancreatic cancer that it is usually considered a preterminal event.

Snady et al., reported on a subgroup of 68 patients with unresectable, invasive T3 tumors was treated with simultaneous split course radiotherapy plus 5-fluorouracil, streptozotocin, and cisplatin (RT-FSP). After RT-FSP, CT showed the tumors to have become downstaged to resectable (T1/T2) in 46cases (68%). Then, EUS examination found that the tumor was resectable (T1/2) in only 22 (32%). Surgical resection was then performed in 20. In addition, unresectable T3 tumor was confirmed surgically in 10 for various reasons; intraoperative radiotherapy was administered in 3 of these. Median survival for all 68 was 24mo; for the 46 resectable by CT, survival was 26mo; for the 22 unresectable by CT, survival was 14mo (p<0.02). Median survival for the 22 resectable by EUS was 33mo. This first group was compared to a contemporary, consecutive group of patients (Group 2) who initially were able to undergo a pancreatoduodenectomy for treatment of pancreatic adenocarcinoma (Tables 5-9). RT-FSP significantly improved survival for patient reliably staged as locally invasive, unresectable, nonmetastatic pancreatic carcinoma (T:3;N:0,1;M:0). For the first time, the expected advantage of an earlier stage as the dominant prognostic factor for pancreatic carcinoma was reversed by initial nonoperative treatment.

Preoperative radiotherapy and chemotherapy followed by resection for locally advanced pancreatic cancer has also been shown by others to be well tolerated. A 60% actuarial 5-year survival was reported for the 11 of 34 patients that were able to undergo resection.

T3 pancreatic tumors respond to chemoradiotherapy. Survival was prolonged by a factor of 3 to 5 times reported conventional median survival times. For T3 tumors considered for resection because of CT demonstrated downstaging after chemoradioterapy, about 50% will still be unresectable on EUS. In these cases EUS influenced management in that it avoided unsuccessful resection attempts in the nearly half of CT "downstaged" tumors that were actually unresectable (T3). The degree of response, resection status, and prognosis can be most accurately evaluated with CT plus EUS. In addition, CA19-9 level appears to have a role in predicting prognosis. Clearly, T3 pancreatic tumors respond to chemoradiotherapy in a manner which can effect management and outcomes shown in the algorithm (Figure 1). EUS plays a key role in monitoring patients treated with chemotherapy and radiotherapy. EUS can assist in evaluating response to combined chemotherapy and radiotherapy and predict resection status of pancreatic tumors. The above studies lend further support to the use of nonoperative treatment as the first line treatment for pancreatic cancer in selected patients. In addition, about 10 to 20% of small <3cm tumors may be bile duct, endocrine or some other tumor where median survival and success of periadjuvant therapy or surgery and combined modality therapy may be double the improved survivals. EUS has been helpful in diagnosis of these types of tumors. Intraoperative LUS is more complex and unlikely to have any significant advantage over preoperative EUS, although no comparative study has yet been reported. Because of its accuracy, convenience and low complication rate, EUS appears likely to replace all other tests as the initial method to evaluate patients diagnosed on clinical signs and laboratory tests as having an endocrine tumor.

Conclusion

Using endoscopic ultrasound imaging, highly accurate pancreatobiliary tumor characterization and staging is now possible without surgery. Precise endosonographic preoperative staging allows use of the TNM pathological staging system to stratify treatment. Endoscopic ultrasonography often establishes a diagnosis in malignant and, in certain patients, benign disease. When a tissue diagnosis is required, endoscopic ultrasonography has a critical role in defining an abnormal area for fine needle aspiration from the gastrointestinal lumen. Endoscopic ultrasonography is unsurpassed in determining resectability of pancreatobiliary neoplasms. It can be used to monitor treatment of downstaged tumors prior to attempted resection. Using endoscopic ultrasonography for earlier diagnosis and precise staging significantly improves the clinical outcome of patients because advances in both surgical techniques and in combined chemotherapy and radiotherapy can be applied selectively.

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Table 1
Accuracy of Pancreatobiliary Tumor Staging and resectability with EUS and CT

Table 2
EUS Accuracy of T staging for Pancreatic Carcinoma

Table 3
Correlation of EUS T stage with the presence of malignant lymph nodes

Table 4
Correlation of T and N stage to survival for Pancreatic Carcinoma

Table 5
Patient Characteristics

Table 6
Survival

Table 7
Treatment Factors Influencing Survival in RT-FSP Group 1

Table 8
Prognostic Factors Influencing Survival in RT-FSP Group 1

Table 9
Prognostic factors on Survival in Primary Resection Group-2