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(Radiology. 1999;213:107-111.)
© RSNA, 1999

Ultrasonography

Abdominal US for Diagnosis of Pancreatic Tumor: Prospective Cohort Analysis1

Britt-Marie Karlson, MD, Anders Ekbom, MD, PhD, Per Gunnar Lindgren, MD, PhD, Vendela Källskog, MD and Jonas Rastad, MD, PhD

1 From the Departments of Surgery (B.M.K., J.R.), Cancer Epidemiology (B.M.K., A.E.), and Diagnostic Radiology (P.G.L., V.K.), University Hospital, S-75185 Uppsala, Sweden; and the Department of Epidemiology, Harvard School of Public Health, Boston, Mass (A.E.). Received September 24, 1997; revision requested November 25; final revision received February 9, 1999; accepted April 4. Address reprint requests to B.M.K. (e-mail: Britt-Marie.Karlson @Kirurgi.uu.se).


   Abstract
TOP
 Abstract
Introduction
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
PURPOSE: To elucidate the accuracy of abdominal ultrasonography (US) in the diagnosis of pancreatic tumors.

MATERIALS AND METHODS: In all patients referred for pancreatic US during 1988–1990, data on malignant disease and survival were analyzed by using the Swedish Death and Cancer Registries. Nine hundred nineteen patients were entered into the analysis. In 140 of them, a clinical diagnosis of tumor in the pancreatic area was confirmed within 1 year after US. These tumors were primary pancreatic tumors (n = 102), common bile duct and duodenal cancers (n = 17), and metastases in the pancreatic area (n = 21).

RESULTS: The sensitivity of US in the detection of all tumors in the pancreatic area was 88.6% (124 of 140 patients), which was similar to that for the detection of exocrine pancreatic cancer, 90% (79 of 88 patients). There were nine false-positive US examinations, for a specificity of 98.8% (770 of 779 patients). Systematic sampling of 94 investigations confirmed an association between US accuracy and presence of clinical symptoms of pancreatic cancer. Significant differences in the sensitivity (P < .05) and accuracy (P < .01) of diagnosis were observed between three experienced investigators.

CONCLUSION: Study results support the use of US as a first-line diagnostic examination in patients suspected of having pancreatic tumor. Dependency on the investigator's experience with US mandates continuous evaluation of its performance.

Index terms: Abdomen, US, 77.1298, 798.1298 • Pancreas, neoplasms, 77.321, 77.33 • Pancreas, US, 77.1298, 77.12985


   Introduction
TOP
 Abstract
 Introduction
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
Pancreatic cancer has a consistent annual incidence of 10.6–12.0 cases per 100,000 Swedish men and women (1). The median survival duration is approximately 4 months after diagnosis, and the prognosis is very poor, even after macroscopically radical resection (2–5). Early diagnosis is important to exclude potentially curable disorders. A sensitivity of 94% in the diagnosis of pancreatic cancer with abdominal ultrasonography (US) has been suggested (6,7), and this modality has been recommended as the primary examination for clinical suspicion of pancreatic cancer (8,9). Others (3,10–13) advocate computed tomography (CT) for this purpose and have had sensitivities below 70% with US. Although this discrepancy may be related to the investigator's level of experience with US (8), confounding findings may also result from the small patient groups examined or restrictions in patient selection. In this prospective study, we examined the accuracy of US in a consecutive cohort of more than 900 patients who underwent abdominal US of the pancreatic area for routine clinical indications. Our purpose was to determine the accuracy of this modality in the diagnosis of pancreatic tumor.


   MATERIALS AND METHODS
TOP
 Abstract
 Introduction
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 References
 
A total of 960 patients underwent US of the pancreas in the department of diagnostic radiology at our institution during 1988–1990. Demographic data included the patient's personal national registration number, which is allocated to all Swedish inhabitants (14), the referring clinic, and a discovery code filed by the investigating physician at the time of the US examination. This code indicated the results of the US examination, including tumor, cyst, inflammation, and normal findings. The patients were referred from all departments of the hospital—particularly, the departments of surgery and medicine, but also the department of oncology—and from general practitioners in the county.

A dynamic 3.5- or 5-MHz sector or linear US scanner (Acuson, Mountain View, Calif) was used. US was performed with interposed water or with the patient in a standing position by some investigators to improve visualization of the pancreas, but the frequency of these procedures was not recorded. The US-based diagnosis of small pancreatic tumors was based on the identification of a poorly reflecting and attenuating pancreatic mass. The larger tumors were more heterogeneous echogenically and exhibited well-defined irregular or lobulated margins. Dilatation of the bile and pancreatic ducts was considered to be an important sign of the presence of pancreatic tumors, but it was never the sole evidence for US-based diagnosis (Figs 1, 2).



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  		Figure 1. Abdominal US scan shows a normal pancreas (1), the confluence between the portal and splenic veins (2), the splenic vein (3), the superior mesenteric artery (4), the inferior vena cava (5), and the aorta (6).

 


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  		Figure 2. Abdominal US scan shows exocrine pancreatic cancer in the head of the pancreas (1). The common bile duct (2) and portal vein (3) also are seen.

 
Linkage to the Swedish Cancer and Death Registries, on the basis of the national registration number, provided access to information on the tumor diagnoses and dates of death in the 960 patients until December 1991. The accuracy of both registries was assessed, and underreporting was determined to be less than 4% (15–17). Verification of the diagnosis of pancreatic cancer in the Cancer Registry was performed by using histologic analysis in 84% of the patients (1).

The Cancer Registry revealed 33 patients with a diagnosis of pancreatic cancer before US was performed. After the exclusion of these individuals and of eight patients with irretrievable US records, the study included 919 patients (489 women [53.2%], 430 [46.8%] men; median age, 58 years) who underwent US of the pancreatic area for any reason. The US investigation revealed tumor in the pancreatic area in 133 patients, whereas the US scan was normal in the remaining 786 patients. The medical charts and US reports of all patients were reviewed; the US discovery code indicated (a) the presence of tumor in the pancreatic area (133 patients), (b) the clinical diagnosis of tumor in the pancreatic area (140 patients), and (c) a systematic sample of every 10th patient in the original cohort (97 patients). Six of the eight patients with irretrievable US records did not have clinically diagnosed tumors. Of the other two patients, one had an insulinoma that was recognized 1 year before US, and the other had a malignant melanoma that was recognized 12 years before US.

Statistical Analyses
The sensitivity of US for the detection of pancreatic tumor was calculated as the proportion of true-positive examinations divided by the number of patients with tumor (as recorded in the Cancer Registry), whereas the specificity was the ratio of true-negative examinations to number of patients without tumor. The positive predictive value was calculated as the number of true-positive examinations divided by the sum of true-positive and false-positive examinations. The negative predictive value was the ratio of true-negative examinations to the sum of true-negative and false-negative examinations. In the statistical analyses, the {chi}2 test was used to calculate proportions, and a P value of less than .05 was considered to be significant.


   RESULTS
TOP
 Abstract
 Introduction
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 References
 
Tumor Diagnosis and Size
Medical charts and linkage to the Swedish Cancer Registry revealed that 140 patients had a diagnosis of tumor in the investigated area within 1 year after US (Table 1). These tumors included exocrine and endocrine primary pancreatic tumors (n = 102) and cancers of the common bile duct, duodenal papilla, and duodenum (n = 17). Confirmation of pancreatic metastasis (n = 21) required a malignant diagnosis in the Cancer Registry and identification with operative excision (n = 5), open or percutaneous core-needle biopsy (n = 7), autopsy (n = 1), or other imaging methods such as computed tomography (CT) and retrograde or transhepatic cholangiography (n = 8).


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  		TABLE 1. Tumor Diagnoses in 140 Patients
 
The mean age of the 88 patients (53 [60%] women, 35 [40%] men) with exocrine pancreatic cancer was 64.7 years; 50 (57%) of them had jaundice at the time of US. One of the patients was falsely entered in the Cancer Registry as having exocrine pancreatic cancer. Autopsy on this patient demonstrated cancer of the gallbladder and a normal pancreas. The patient remained in the analysis, however, because entrance in the Cancer Registry was the selected end point of the study. Among the remaining 87 patients, the tumor was located in the head (64 patients), body (16 patients), or tail (five patients) of the pancreas. The entire pancreas was involved in two patients. The diameter of the tumors at US was recorded in 70 patients and was described as "large" in another eight. The recorded mean size of the tumors was 4.0 cm; the mean tumor size in the head of the pancreas was 4.0 cm (range, 1.0–10.0 cm); in the body, 3.5 cm (3.0–7.0 cm); and in the tail, 4.4 cm (3.0–7.0 cm).

The diagnosis of absence of tumor in the pancreatic area (779 patients) was established after follow-up in the Swedish Cancer Registry for a minimum of 2 years after US or until death from other causes. Altogether, 258 patients died during the follow-up period; these patients included 114 (81.4%) of the 140 patients with a clinical diagnosis of any tumor in the pancreatic area and 85 (97%) of the 88 patients with exocrine pancreatic cancer. None of the other 144 deaths could be attributed to such tumors.

In 15 of the patients with exocrine pancreatic cancer, other abdominal examinations were performed before US. These examinations were CT in seven patients, US of the pancreas in six patients, endoscopic retrograde cholangiopancreatography in one patient, and laparotomy in one patient.

Efficiency of US in the Patient Cohort
US demonstrated tumors in the pancreatic region in 124 of the 140 patients with subsequent confirmation of such a neoplasm (Table 2), for a sensitivity of 88.6%. The sensitivity of US in the detection of exocrine pancreatic cancer was similar: 79 of 88 patients (90%) were shown to have this cancer. In the entire group of patients without tumor, nine examinations were falsely positive, for a specificity of 98.8% (770 of 779 patients). The medical charts of the patients with false-positive examination results revealed final diagnoses of pancreatitis (n = 5), pancreatic cyst (n = 1), and no signs of disease (n = 3).


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  		TABLE 2. US Findings in the 919 Patients in Relation to Clinical Diagnosis of Any Tumor in the Pancreatic Area and of Exocrine Pancreatic Cancer
 
In 16 patients, either the US scan was false-negative (n = 15) or the scan of the pancreas was not available (n = 1); thus, cancers of the following areas were missed: exocrine pancreas (n = 9), common bile duct (n = 5), and duodenal papilla (n = 2). The positive predictive value and negative predictive value of US for the detection of all tumors in the pancreatic area were 93.2% (124 of 133 patients) and 98.0% (770 of 786 patients), respectively. The missed pancreatic cancers were diagnosed within 2 months after the US examination by using CT in two patients, another US examination in one patient, laparotomy in four patients, autopsy in one patient, and an unknown procedure in one patient. All of these patients died within 6 months after US. Their US findings were interpreted as pancreatitis in five patients, pseudocyst in one patient, normal in two patients, and an incompletely visualized pancreas in one patient. The individuals with an ultrasonographically normal pancreas included the patient with gallbladder cancer who was falsely registered. The results of autopsy on another patient revealed the pancreas to be normal macroscopically but with apparent cancer microscopically. The sizes of the missed pancreatic cancers were 4–10 cm.

Cohort Sample
A total of 94 records of the systematically selected US examinations could be retrieved; 19 were those of patients who had a subsequent clinical diagnosis of tumor in the pancreatic area. In three (3%) of the 94 investigations, the pancreas could not be visualized. Thirteen sonologists (including P.G.L. and V.K.) performed up to 30 of these examinations each. Three of these sonologists (one of which was P.G.L.) performed 69 (73%) of the 94 examinations and were classified as experienced. The others performed one to five examinations each and were often supervised by the experienced investigators. The referring physician specifically requested that the patient be evaluated for the possible presence of tumor in 53 (56%) of the cases (Table 3). Twenty-five (27%) of the 94 patients had a medical history that suggested pancreatic cancer, that is, they had experienced painless jaundice, anorexia, or loss of appetite with vomiting (3,4,18–20).


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  		TABLE 3. Distribution of Two Clinical Indications for US between Experienced and Nonexperienced Sonologists in the Systematic Sample of 94 Investigations
 
The specific request to check for tumor by the referring physician was not found to be related to the efficiency of US in the detection of pancreatic cancer, whereas the opposite was true with regard to suggestive medical history (Table 4). The US findings in the systematically selected sample revealed that neither the specific request to check for tumor nor the history of common symptoms of pancreatic cancer influenced the choice of experienced versus nonexperienced sonologist (Table 3). There were significant differences between the three experienced sonologists with respect to both the accuracy of a positive tumor finding (P < .01) and the sensitivity for detection of pancreatic cancer (P < .05) (Table 5).


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  		TABLE 4. Outcome of Pancreatic US in Relation to Two Clinical Indications for US in the Patients with Exocrine Pancreatic Cancer
 

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  		TABLE 5. Comparison of the Three Experienced Sonologists with Respect to the Accuracy of US in the Patients with Any Tumor in the Pancreatic Area and Those with Pancreatic Cancer
 

   DISCUSSION
TOP
 Abstract
 Introduction
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
References
 
In this prospective study, we evaluated abdominal US of the pancreatic area, with an independent assessment of outcome through the Swedish Cancer and Death Registries. The consecutive recruitment of a substantial number of patients referred for US for any clinical indication ensured an unbiased selection of patients in the age group that is characteristic for diseases of the pancreatic area. In the systematic sample of US investigations, 41 (44%) of the 94 patients had no specified indication that was suspicious for cancer nor any symptom that was characteristic of pancreatic cancer. Thus, the sensitivity and specificity of US for the detection of pancreatic and peripancreatic tumors and the accuracy of both the positive and negative findings could be determined in a clinically relevant setting.

There were, however, potential limitations of the study design. The motivation to refer patients for US might differ among centers, and this factor might reduce the validity of our conclusions. Important determinants in this respect may include the availability of US and the subjective estimates of its efficiency. Consistent with the findings in the present study and with those of previous studies (5–9,21,22), a generally liberal attitude toward US appears to prevail during patient recruitment. Another limiting aspect is related to the fact that US and clinical records were retrieved for only those patients who had a US discovery code of tumor or a clinical diagnosis of cancer in the pancreatic area. The results from the systematic sample revealed that three (3%) of the 97 US reports could not be retrieved because of record failures. There were no diagnostic inconsistencies, however, when the computed discovery codes and the available US records were compared.

Metastases to the pancreatic area should be contemplated, and, consistent with the findings in the present study, constitute a clinical reality and may originate from a variety of malignancies (23–25). In this study, the presence or absence of such spreading essentially remained unverified after a normal US examination, because the records of patients with clinically diagnosed nonpancreatic cancers were not routinely reviewed. All metastases were identified by using histologic analysis or other imaging methods that are commonly performed in patients with pancreatic neoplasms. Finally, the duration of follow-up in this study may be too short, even for the highly malignant tumors that occur in the pancreatic area, because symptoms of pancreatic cancer may prevail for several years prior to diagnosis (26–29).

The results of the current evaluation support the usefulness of US in the diagnosis of pancreatic tumors (6–9). A sensitivity of 88.6% (124 of 140 patients) in the detection of any pancreatic or peripancreatic tumor was attained, and similar efficiency was noted in the detection of exocrine pancreatic cancer. Substantially less impressive values have been reported previously (3,10–13), but some of these studies included examinations that were performed by radiologic trainees (10). The differences in accuracy among the sonologists in this study might help to explain the previous contradictory results, because US findings are difficult to interpret.

The experience of the investigating sonologist chosen was unrelated to the referring clinician's specific concerns regarding the presence of pancreatic tumor and to the history of symptoms characteristic of pancreatic cancer. The experienced sonologists exhibited significant variation in their ability to recognize pancreatic cancer and other tumors in the pancreatic area. Because the nonexperienced sonologists generally were supervised while performing examinations, evaluation of their personal performances was not possible.

The efficiency of US was related to the presence of symptoms commonly associated with pancreatic cancer, whereas we found no relationship between US efficiency and the specific request to examine for tumor on the referral note; these findings may have contributed to the differences in the reliability of US between studies. A possible explanation may be related to the dependence of such symptoms on tumor size and location or to other factors that increase US-based detection such as anatomic features that affect echogenicity and delineation of tumor.

In conclusion, the results of this study support the general recommendation to use US for primary imaging in patients who are suspected of having pancreatic tumor (6–9), because of the efficiency, availability, and noninvasiveness of this modality. With US guidance, biopsy can be used, with minimal risk of complications, to confirm diagnosis without resorting to surgery and to identify endocrine pancreatic neoplasms that are amenable to treatment even at more advanced stages (8,30–34). The dependency on investigator experience with US compared with other methods, however, mandates local evaluation of the performance of US both before and after it is introduced as the primary imaging strategy in the clinical management of pancreatic tumors.


   Footnotes
 
Author contributions: Guarantor of integrity of entire study, B.M.K.; study concepts, B.M.K., J.R.; study design, B.M.K., A.E., J.R., P.G.L.; definition of intellectual content, B.M.K., J.R., A.E.; literature research, B.M.K.; clinical studies, P.G.L., V.K.; data acquisition, B.M.K., V.K.; data and statistical analyses, B.M.K.; manuscript preparation, B.M.K., A.E., J.R.; manuscript editing, B.M.K., A.E., J.R., P.G.L.; manuscript review, all authors.


   References
TOP
 Abstract
 Introduction
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 

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