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(Radiology. 1999;211:211-214.)
© RSNA, 1999

Gastrointestinal Imaging

Colon Cancer at Barium Enema Examination and Colonoscopy: A Study from the County of Hordaland, Norway1

Eivind Strøm, MD and John L. Larsen, MD, PhD

1 From the Department of Radiology, University Hospital of Bergen, Haukeland Hospital, N-5021 Norway. Received December 22, 1997; revision requested March 10, 1998; revision received August 7; accepted October 26. Supported in part by the legacy of the Blix family. Address reprint requests to E.S.


   Abstract
TOP
 Abstract
Introduction
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
PURPOSE: To evaluate the efficacy of barium enema examination as routinely performed in the detection of colon cancer in the inhabitants of a well-defined and circumscribed geographic region.

MATERIALS AND METHODS: The study comprised 571 patients with histopathologically verified colon cancer during 1990–1993 from the county of Hordaland. The barium enema examination results were reviewed retrospectively.

RESULTS: The correct diagnosis was reached in 351 cases (sensitivity, 90.9%) in 386 tumor locations on the basis of the results of 381 barium enema examinations. Cancer or an important precancerous lesion was overlooked in 26 cases (6.7%), and the examination was not feasible in nine cases (2.3%). The correct diagnosis was reached in 172 cases (sensitivity, 80.0%) in patients with 215 tumor locations on the basis of the results of 213 colonoscopies. Cancer or an important precancerous lesion was overlooked in 13 cases (6.0%). The examination was technically not successful (ie, the affected area was not reached with the scope) in 30 cases (13.9%).

CONCLUSION: Barium enema examination is valuable in the diagnosis of colon cancer and compares favorably with colonoscopy. The main reason for missed radiologic diagnosis is failure to observe important lesions visible on the radiographs.

Index terms: Barium enema examination, 75.1281, 75.1282 • Colon, neoplasms, 75.321 • Colon, radiography, 75.1281, 75.1282 • Colonoscopy, 75.129 • Efficacy study


   Introduction
TOP
 Abstract
 Introduction
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
Colorectal carcinoma is among the most common cancers in the Western world, and in Norway it is the second most common in both women and men after breast cancer and prostate cancer, respectively (1). Despite the increased use of colonoscopy in Norway to about 27,000 examinations every year, the procedure is outnumbered by the 40,000 barium enema examinations performed (2). Barium enema examination is still the most important tool used in the detection of colon tumors in Norway, whereas rectal tumors are diagnosed mainly by means of rectoscopy.

Previous investigations (3–5) concerning the accuracy of barium enema examination in the detection of colon neoplasms have shown a wide range of sensitivity and specificity. Perusal of the pertinent literature demonstrates that this discrepancy may to a large extent be caused by different selections of the population under study. To reflect the value of routine barium enema examinations in an unselected population, we performed a retrospective investigation encompassing diagnostic studies performed during 3 years in patients with histopathologically certified carcinomas within the county of Hordaland in western Norway.

The 3-year time span was chosen for practical reasons; older material will not always be available. The objection could be made that a 3-year interval between the histopathologic identification of the cancer and the diagnostic examination will mean that the more rapidly growing tumors will lead to overestimation of the insensitivity of the applied diagnostic methods. A closer analysis of our material does, however, make this objection negligible.

Our purpose was to evaluate the efficacy of barium enema examination as routinely performed in the detection of colon cancer in the inhabitants of a well-defined and circumscribed geographic region and to compare barium enema examination with colonoscopy in the same geographic region and explore the reasons for missed radiologic diagnoses.


   MATERIALS AND METHODS
TOP
 Abstract
 Introduction
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 References
 
We received personal identification data from the National Cancer Registry of Norway regarding all cases of histopathologically verified cancer of the colon reported in the five hospitals (Haukeland University Hospital, Bergen; Diakowissehjemmets Hospital Haraldsplass, Bergen; Stord County Hospital; Voss County Hospital; Odda County Hospital) in the county of Hordaland, Norway, during the 4 years 1990–1993. Medical records were also obtained from two private clinics (Betanien Hospital, Fyllingsdalen; Bergen Röntgeninstitutt, Bergen) and one private medical center (Christen J. Bang, Nesttun). Only patients who had the diagnosis confirmed by means of histopathologic findings were included in the study. Suspected but not proved cases were excluded. The radiologic and the colonoscopic reports were supplied by the institutions where the examinations had been performed.

The region of Hordaland has approximately 430,000 inhabitants, amounting to one-tenth of the Norwegian population (6). We included only cases with complete histopathologic and radiologic or colonoscopic records, with a total of 581 tumors in 571 patients. Ten patients (five men and five women) had two simultaneous tumors in different locations. We recorded whether the patients had undergone barium enema examination or colonoscopy within the past 3 years before the histopathologic diagnosis and the results of these examinations as stated in the patients' records. The supposed nature of the lesion and its location were recorded, and the information given was compared to the final results. Barium enema examination was performed in 381 patients, and colonoscopy was performed in 213 patients.

The radiographs for all false-negative radiologic studies were reviewed by two radiologists (E.S., J.L.L.) who had access to the surgical findings, histopathologic findings, and autopsy results. Neither of these two radiologists had personally examined any of the included patients. Because the main reason for a false-negative diagnosis in the barium enema examinations was missed perception of an apparent lesion, reexamination of the radiographs did not lead to interobserver variation between the authors. In 239 of the tumor locations, single-contrast barium enema examinations were performed, and in 147 locations the double-contrast technique was used.

The age distribution of the patients is shown in Table 1. As expected, there was a marked increase in cancer in the older age groups. Of the 571 patients, there were 315 women (55%) and 256 men (45%).


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  		TABLE 1. Age Distribution of Patients
 
The barium enema examinations were performed in one university hospital, four local hospitals, and two private clinics. In addition, colonoscopy was performed at the five hospitals and one private medical center. This allowed evaluation of the daily performances of a large number of physicians. The retrospective approach provided the opportunity to test the methods as practiced under normal circumstances without interfering with the daily workload of the departments or inspiring the diagnosticians to make extraordinary efforts.


   RESULTS
TOP
 Abstract
 Introduction
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 References
 
In barium enema examinations in 381 patients, the correct diagnosis was reached for 351 of 386 tumors (sensitivity, 90.9% [351 of 386]) (Table 2). Cancer or a precancerous lesion was overlooked in 26 cases (6.7%). The examination was technically not possible in nine cases (2.3%), most of these being caused by the inability of the patient to cooperate. The distribution of the tumors is shown in Table 3. Previous investigators (7) found a redistribution in the location of colon cancers, with more malignancies in the proximal part of the bowel in recent years than in earlier years. This agrees with our study in which more than one-third (37.9%) were located in the cecum, ascending colon, or ileocecal junction (Table 3). Tumors of the rectum were not included in the present study.


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  		TABLE 2. Results of Barium Enema Examinations in 381 Patients with 386 Tumors
 

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  		TABLE 3. Distribution of Tumors Diagnosed at Barium Enema Examination
 
In colonoscopies in 213 patients with 215 tumors, the correct diagnosis was reached in 172 cases (sensitivity, 80.0% [172 of 215]) (Table 4). Cancer or a definite precancerous lesion was not found in 13 cases (6.0%), even though the region of involvement was reportedly reached by the endoscopist. The examination was technically not successful (ie, the affected area was not reached with the scope) in 30 cases (13.9%).


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  		TABLE 4. Results of Colonoscopic Examinations in 213 Patients with 215 Tumors
 
Of the 26 barium enema examinations in which cancer was overlooked, the radiographs were available for retrospective evaluation in 23 patients and missing in three patients (Table 5). Fifteen examinations were double contrast, and 11 were single contrast. Because 239 of the barium enema examinations were single contrast and 147 were double contrast, sensitivities of 95.4% (228 of 239) and 89.8% (132 of 147), respectively, were found. Two patients had two tumors each, one of which was correctly diagnosed and one of which was overlooked (Table 6).


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  		TABLE 5. Barium Enema Examinations with Overlooked Tumors
 

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  		TABLE 6. Comparison of Techniques for Found and Overlooked Tumors at Various Locations
 

   DISCUSSION
TOP
 Abstract
 Introduction
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
References
 
Carcinoma of the colon is a potentially curable disease, highly dependent on early diagnosis. It is therefore important to perform quality controls of the diagnostic methods used and to pinpoint fallacies and institute measures to prevent them. The present multicenter study reflects the situation in Norway, where radiologic education and practice is uniform. In conformity with previous investigators (8–12), we found perceptive errors to be the most frequent cause of false-negative diagnosis.

Because many radiologists in Norway perform their examinations and interpret their findings alone, double or triple reading of the radiographs is uncommon. These methods have been shown to increase the efficacy of barium enema examination substantially (10,11). However, simple arithmetic shows that double reading of the 40,000 barium enema examinations, each requiring 6 minutes, performed in Norway every year would amount to 4,000 hours, or approximately the workload of two experienced radiologists.

As Rice (3) points out, it is likely that there exists a huge discrepancy in quality between published reports and everyday practice, at least in the United States in both academic institutions and private practice. The design of the present study was, therefore, retrospective to avoid interference with examination practice and to reflect the everyday practice of Norwegian radiologists.

Even though double or triple reading is not usual in Norway, the study demonstrates the high quality of the barium enema examinations, considering that this is a study of nonselected investigators or institutions. Especially encouraging is the fact that technical factors alone or combined with error of perception contributed to only nine of the 23 overlooked tumors with radiographs available (Table 5), demonstrating that the technical training of the radiologists has been adequate.

It can be argued that a malignant tumor may have developed in the interval between the barium enema examination and the detection of the tumor, thus giving the examination a false low sensitivity. As Table 5 shows, however, 13 patients had radiographs showing a tumor that was not detected at the first reading. Technical and combined (technical and perceptual) errors in nine patients had a delay in tumor discovery of 15, 15, 11, 4, 1, 1, 0, 0, and 0 months. The last four patients of Table 5, one with nonvisualization of the tumor and three with missing radiographs, had their tumors discovered 20, 4, 3, and 2 months after their first barium enema examination. It is thus likely that no more than four patients could have possibly developed a malignant growth during the delay time.

When analyzing the possibility of tumor originating between the barium enema examination and the definitive diagnosis in four cases, we discovered that in the first case there were 6 months between barium enema examination and a colonoscopic examination that showed a 3-cm tumor in the sigmoid colon. In the second case, the time span was 1 month before a tumor in the descending colon was discovered at colonoscopy, and the third case had a time lapse of 15 months before a repeated barium enema examination showed a polypous tumor in the cecum. In the fourth case, the patient underwent surgery 2 days after the barium enema examination, and in addition to the originally detected tumor, a cancerous polyp was found in the transverse colon.

The present study findings support earlier evidence (8,9) that tumors located in the proximal part of the colon are overlooked more easily than tumors located in the distal part of the colon. This fact needs to be emphasized when educating radiologists.

When evaluating the effects of overlooked tumors, we found that the available data are sparse, but Bolin et al (13) calculated the doubling time of colon cancer to be 195–620 days. Nevertheless, a subgroup of colon cancers with a very rapid growth rate seems to exist (14). Patients who are clinically suspected of having cancer and who have negative barium enema examination or colonoscopic examination results should therefore be reexamined early.

It is not possible for us to make unambiguous comparisons of quality between the results of double- and single-contrast barium enema examinations for a variety of reasons; the two techniques tended to be used in different patient groups with distinct clinical problems. In some cases, a combination of techniques was used, and double-contrast barium enema examination was used more often in younger, better cleansed, and potentially healthier patients. In contrast, the usual routine was to use single-contrast barium enema examination in older patients, or in an acute situation, such as when trying to visualize the cause of an acute obstruction of the large bowel. Neither does the study allow a randomized comparison of barium enema examination versus colonoscopy, again owing to different patient populations, but it does show how the different methods compare when used in daily routines.

Regarding colonoscopy, it is important to stress that an examination in which the cecum and the ascending colon are not visualized should be followed promptly by a barium enema examination. The fact that most patients suspected of having carcinoma of the colon find colonoscopy much more disagreeable (15) should also be taken into account when deciding which diagnostic strategy to follow. Furthermore, the radiographs of the barium enema examination are available for a second opinion by another diagnostician if necessary, whereas colonoscopic examination findings are only subjectively documented. Barium enema examination involves only a small risk of perforation (0–4 cases per 10,000 examinations), whereas this risk is greater for colonoscopy (10–20 cases per 10,000 examinations) (4). The main advantages of colonoscopy are the ability to remove polyps and perform biopsy of undetermined lesions. It was previously thought that most cancers evolved from polyps, but this theory is now much disputed (16).

Economic factors should also be taken into consideration. In Norway, the government pays the main part of the health expenses, and the prices are low. The cost of diagnostic colonoscopy in Norway is NKr 825 (U.S. $110), whereas the fee for a single- or double-contrast barium enema examination is NKr 500 (U.S. $65) or NKr 650 (U.S. $85), respectively; the difference in cost between these examinations is usually greater in other countries. Both the diagnostic results presented in this study and economic factors provide a good case for barium enema examination as a suitable tool for the diagnosis of colon cancer. In conclusion, routinely performed barium enema examinations are effective in the diagnosis of colon cancer and can in this respect compete with colonoscopy. Perceptual errors are the main cause of misdiagnosis.


   Acknowledgments
 
We thank Sally Tveit for invaluable help in preparing the manuscript.


   Footnotes
 
Author contributions: Guarantors of integrity of entire study, E.S., J.L.L.; study concepts, J.L.L.; study design, J.L.L., E.S.; definition of intellectual content, E.S., J.L.L.; literature research, E.S., J.L.L.; data acquisition and analysis, E.S.; manuscript preparation, editing, and review, E.S., J.L.L.


   References
TOP
 Abstract
 Introduction
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 

  1. Kreftsregisteret . Cancer in Norway 1992: the Norwegian Cancer Society Institute for epidemiological cancer research Oslo, Norway: Landsforeningen mot kreft, 1995; 3-118.
  2. Hoff G. Kontroller til besvær. Tidsskr Nor Laegeforen 1994; 114:553-554.[Medline]
  3. Rice R. Lowering death rates from colorectal cancer: challenge for the 1990s. Radiology 1990; 176:297-301.[Free Full Text]
  4. MacCarty R. Colorectal cancer: the case for barium enema. Mayo Clin Proc 1992; 67:253-257.[Medline]
  5. Smith C. Colorectal cancer: radiologic diagnosis. Radiol Clin North Am 1997; 35:439-456.[Medline]
  6. . Statistical yearbook of Norway Oslo, Norway: Statistisk sentralbyrå, 1995.
  7. Cady B, Stone M, Wayne J. Continuing trends in the prevalence of right-sided lesions among colorectal carcinomas. Arch Surg 1993; 128:505-509.[Abstract]
  8. Bolin S, Franzen L, Nilsson E, Sjödahl R. Carcinoma of the colon and rectum: tumors missed by radiologic examination in 61 patients. Cancer 1988; 61:1999-2008.[Medline]
  9. Anderson N, Cook H, Coates R. Colonoscopically detected colorectal cancer missed on barium enema. Gastrointest Radiol 1991; 16:123-127.[Medline]
  10. Markus J, Somer S, O'Malley B, Stevenson G. Double-contrast barium enema studies: effect of multiple reading on perception error. Radiology 1990; 175:155-156.[Abstract/Free Full Text]
  11. Brady A, Stevenson G, Stevenson I. Colorectal cancer overlooked at barium enema examination and colonoscopy: a continuing perceptual problem. Radiology 1994; 192:373-378.[Abstract/Free Full Text]
  12. Barloon T, Shumway J. Medical malpractice involving radiologic colon examinations: a review of 38 recent cases. AJR 1995; 165:343-346.[Abstract/Free Full Text]
  13. Bolin S, Nilsson E, Sjödahl R. Carcinoma of the colon and rectum: growth rate. Ann Surg 1983; 198:151-158.[Medline]
  14. Burnett K, Greenbaum E. Rapidly growing carcinoma of the colon. Dis Colon Rectum 1981; 24:282-286.[Medline]
  15. Steine S. The use of double-contrast barium enema in an outpatient clinic: referrals, diagnostic outcome, and patients' experiences of pain. Thesis Oslo, Norway: Department of General Practice, University of Oslo, 1993.
  16. Stelzner F. Sequential cancer or concomitant cancer. Zentralbl Chir 1992; 117:471-475.[Medline]



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