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Is There Still a Role for Double-Contrast Barium Enema Examination?

2008; Elsevier BV; Volume: 6; Issue: 4 Linguagem: Inglês

10.1016/j.cgh.2007.12.051

1542-7714

Cheri L. Canon,

Gastric Cancer Management and Outcomes

The role of double-contrast barium enema examination (DCBE) in screening for colorectal carcinoma has evolved considerably in recent years. This review will discuss the current indications for DCBE and contrast fluoroscopy of the colon and the anticipated future role of these studies. The role of double-contrast barium enema examination (DCBE) in screening for colorectal carcinoma has evolved considerably in recent years. This review will discuss the current indications for DCBE and contrast fluoroscopy of the colon and the anticipated future role of these studies. Along with fecal occult blood testing (FOBT), sigmoidoscopy, and conventional optical colonoscopy (OC), double-contrast barium enema examination (DCBE) has been an important screening tool for colorectal carcinoma (Figure 1). Guiding principles of a successful screening program include accurate diagnosis of disease in its early state (asymptomatic patient) with low risk to the patient and low cost to society. Although there have been numerous studies evaluating the accuracy of DCBE, no prospective evaluation has been performed in a screening population, thus inserting bias. In a meta-analysis of 25 studies evaluating DCBE performance, Glick et al1Glick S. Wagner J.L. Johnson C.D. Cost-effectiveness of double-contrast barium enema in screening for colorectal cancer.AJR. 1998; 170: 629-636Crossref PubMed Scopus (79) Google Scholar reported sensitivity ranging from 85%–95%, approaching that of OC. On the other hand, the National Polyp Study reported a sensitivity of 48% for polyps 10 mm and larger,2Winawer S.J. Stewart E.T. Zauber A.G. et al.A comparison of OC and double-contrast barium enema for surveillance after polypectomy.N Engl J Med. 2000; 342: 1766-1772Crossref PubMed Scopus (526) Google Scholar suggesting DCBE is an unacceptable screening strategy. Next to FOBT, DCBE is the safest established screening method, with a reported perforation rate of 1 in 25,0003Blakeborough A. Sheridan M.B. Chapman A.H. Complications of barium enema examinations: a survey of UK consultant radiologists 1992 to 1994.Clin Radiol. 1997; 52: 142-148Abstract Full Text PDF PubMed Scopus (70) Google Scholar versus 2 in 1000 for OC.4Anderson M.L. Pasha T.M. Leighton J.A. Endoscopic perforation of the colon: lessons from a 10-year study.Am J Gastroenterol. 2000; 95: 3418-3422Crossref PubMed Google Scholar, 5Gazelle G.S. McMahon P.M. Scholz F.J. Screening for colorectal cancer.Radiology. 2000; 215: 327-335Crossref PubMed Scopus (48) Google Scholar DCBE is probably cost-effective,1Glick S. Wagner J.L. Johnson C.D. Cost-effectiveness of double-contrast barium enema in screening for colorectal cancer.AJR. 1998; 170: 629-636Crossref PubMed Scopus (79) Google Scholar but because of lack of consensus concerning DCBE performance, application of cost-effective models is difficult. Many referring clinicians are not convinced of DCBE’s value in colorectal screening. In a national survey of radiologists and primary care physicians, 75% of radiologists rated DCBE as an effective screening tool versus 33% of primary care physicians.6Klabunde C.N. Jones E. Brown M.L. et al.Colorectal cancer screening with double-contrast barium enema: a national survey of diagnostic radiologists.AJR. 2002; 179: 1419-1427Crossref PubMed Scopus (19) Google Scholar Furthermore, only 2% of primary care physicians most often recommend DCBE either alone or combined with sigmoidoscopy. As a result, the recent decade has seen a downward trend in DCBE as a screening tool, hastened with the emergence of CT colonography (CTC). Initial studies evaluating efficacy of CTC in symptomatic patients were optimistic,7Fenlon H.M. Nunes D.P. Schroy III, P.C. et al.A comparison of virtual and conventional OC for the detection of colorectal polyps.N Engl J Med. 1999; 341: 1496-1503Crossref PubMed Scopus (676) Google Scholar, 8Yee J. Akerkar G.A. Hung R.K. et al.Colorectal neoplasia: performance characteristics of CT colonography for detection in 300 patients.Radiology. 2001; 219: 685-692Crossref PubMed Scopus (457) Google Scholar but subsequent studies were less so,9Cotton P.B. Durkalski V.L. Palesch Y.Y. et al.Virtual OC: final results from a multicenter study.Gastrointest Endosc. 2003; 57: AB174Abstract Full Text Full Text PDF Scopus (113) Google Scholar, 10Johnson C.D. Harnsen W.S. Wilson L.A. et al.Prospective blinded evaluation of computed tomographic colonography for screen detection of colorectal polyps.Gastroenterology. 2003; 125: 311-319Abstract Full Text Full Text PDF PubMed Scopus (313) Google Scholar and a large study comparing DCBE, CTC, and OC in a symptomatic patient population found OC to be more sensitive.11Rockey D.C. Paulson E. Niedzwiecki D. et al.Analysis of air contrast barium enema, computed tomographic colonography, and OC: prospective comparison.Lancet. 2005; 365: 305-311Abstract Full Text Full Text PDF PubMed Scopus (457) Google Scholar In this study, the performance statistics of DCBE were poor, with a per-patient sensitivity for polyps 10 mm or larger of 48%. A subsequent study of this patient population revealed that 65% of missed polyps on DCBE were due to technical errors (82%), suggesting radiologists need to give greater attention to the performance of DCBE.12Thompson W.M. Foster W.L. Paulson E.K. et al.Causes of errors in polyp detection at air-contrast barium enema examination.Radiology. 2006; 239: 139-148Crossref PubMed Scopus (5) Google Scholar Another study similarly reported no improvement with double reading DCBE, also suggesting technical errors outweighing perceptual errors.13Canon C.L. Smith J.K. Morgan D.E. et al.Double reading of barium enemas: is it necessary?.AJR. 2003; 181: 1607-1610Crossref PubMed Scopus (14) Google Scholar The largest prospective study evaluating CTC in a screening population demonstrated CTC comparable to OC.14Pickhardt P.J. Choi J.R. Hwang I. et al.Computed tomographic virtual OC to screen for colorectal neoplasia in asymptomatic adults.N Engl J Med. 2003; 349: 2191-2200Crossref PubMed Scopus (1735) Google Scholar Preliminary results of the National CT Colonography Trial, presented at the September 2007 meeting of the American College of Radiology Imaging Network, demonstrated similar findings, with CTC accuracy approaching that of OC (unpublished data). Even more important, patients preferred CTC15Gluecker T.M. Johnson C.D. Harmson W.S. et al.Colorectal cancer screening with CT colonography, OC, and double-contrast barium enema examination: prospective assessment of patient perceptions and preferences.Radiology. 2003; 227: 378-384Crossref PubMed Scopus (260) Google Scholar or OC16Bosworth H.B. Rockey D.C. Paulson E.K. et al.Prospective comparison of patient experience with colon imaging tests.Am J Med. 2006; 119: 791-799Abstract Full Text Full Text PDF PubMed Scopus (65) Google Scholar to DCBE. CTC is quickly gaining ground, and some believe it will likely replace DCBE.17Ferrucci J.T. Double-contrast barium enema: use in practice and implications for CT colonography.AJR. 2006; 187: 170-173Crossref PubMed Scopus (32) Google Scholar Therefore, is there a future for barium enema examination? For now, there is a continued role for DCBE in high-risk colonoscopy patients as well as for those with incomplete OC. The published rate of incomplete OC examination ranges from 4%–25%,18Anderson M.L. Heigh R.I. McCoy G.A. et al.Accuracy of assessment of the extent of examination by experienced colonoscopists.Gastrointest Endosc. 1992; 38: 560-563Abstract Full Text PDF PubMed Scopus (73) Google Scholar, 19Dafnis G. Blomqvist P. Pahlman L. et al.The introduction and development of OC within a defined population in Sweden.Scand J Gastroenterol. 2000; 35: 765-771Crossref PubMed Scopus (21) Google Scholar, 20Marshall J.B. Barthel J.S. The frequency of total OC and terminal ileal intubation in the 1990s.Gastrointest Endosc. 1993; 39: 518-520Abstract Full Text PDF PubMed Scopus (221) Google Scholar, 21Winawer S.J. Fletcher R.H. Miller L. et al.Colorectal cancer screening: clinical guidelines and rationale.Gastroenterology. 1997; 112: 594-642Abstract Full Text Full Text PDF PubMed Scopus (1834) Google Scholar whereas the diagnostic yield of the completion barium enema examination after failed OC is just greater than 3%.22Chong A. Shah J.N. Levine M.S. et al.Diagnostic yield of barium enema examination after incomplete OC.Radiology. 2002; 223: 620-624Crossref PubMed Scopus (33) Google Scholar Most completion DCBEs are successfully performed, and one study identified significant additional information in 14% of patients.23Brown A.L. Skehan S.J. Greaney T. et al.Value of double-contrast barium enema performed immediately after incomplete OC.AJR. 2001; 176: 943-945Crossref PubMed Scopus (30) Google Scholar Most failed colonoscopies are attributed to redundancy of the colon or diverticular disease, both of which can be addressed with DCBE. Failed OC because of incomplete bowel preparation warrants a follow-up DCBE, but this should be done at a later time after a repeat, hopefully adequate bowel preparation. However, not all agree on the validity of completion DCBE. Martinez et al24Martinez F. Kondylis P. Reilly J. Limitation of barium enema performed as an adjunct to incomplete OC.Dis Colon Rectum. 2005; 48: 1951-1954Crossref PubMed Scopus (13) Google Scholar have questioned the reliability of performing DCBE in this setting, arguing that although DCBE can be performed to “completion,” the technical adequacy is questionable. Prescribed bowel preparation for patients with incomplete OC and completion DCBE is problematic; there is no agreement as to the most effective bowel preparation.25Ell C. Fischbach W. Keller R. et al.A randomized, blinded, prospective trial to compare the safety and efficacy of three bowel-cleansing solutions for OC.Endoscopy. 2003; 35: 300-304Crossref PubMed Scopus (126) Google Scholar, 26O’Donovan A.N. Somers S. Farrow R. et al.A prospective blinded randomized trail comparing oral sodium phosphate and polyethylene glycol solutions for bowel preparation prior to barium enema.Clin Radiol. 1997; 52: 791-793Abstract Full Text PDF PubMed Scopus (14) Google Scholar, 27Poon C.M. Lee D.W. Mak S.K. et al.Two liters of polyethylene glycol-electrolyte lavage solution versus sodium phosphate as bowel cleansing regimen for OC: a prospective randomized controlled trial.Endoscopy. 2005; 34: 560-563Crossref Scopus (71) Google Scholar, 28Rapier R. Houston C. A prospective study to assess the efficacy and patient tolerance of three bowel preparations for OC.Gastroenterol Nurs. 2006; 29: 305-308Crossref PubMed Scopus (34) Google Scholar, 29Tan J.J.Y. Tjandra J.J. Which is the optimal bowel preparation for OC: a meta-analysis.Colorectal Dis. 2006; 8: 247-258Crossref PubMed Scopus (173) Google Scholar In a meta-analysis of 29 randomized controlled trials between 1990 and 2005 evaluating the effectiveness of sodium phosphate and polyethylene glycol, sodium phosphate was more effective in bowel cleansing,29Tan J.J.Y. Tjandra J.J. Which is the optimal bowel preparation for OC: a meta-analysis.Colorectal Dis. 2006; 8: 247-258Crossref PubMed Scopus (173) Google Scholar although this could be a result of patients having more difficulty completing the large volume polyethylene glycol preparation. Yet, many endoscopists use a “wet” bowel preparation with polyethylene glycol agents. This is not optimal for performance of DCBE, because it results in poor mucosal coating. If it is used, at least 12- to 18-hour delay with a stimulant cathartic should be incorporated to reduce retained fluid30Smith C. Colorectal cancer.Radiol Clin North Am. 1997; 35: 439-456PubMed Google Scholar before undertaking the DCBE. In many institutions, gastroenterologists have adopted a “dry prep,” sodium phosphate or magnesium citrate, regimen because it is better tolerated by most patients and also allows for an adequate DCBE on the same day in the cases of failed OC. This is not recommended in patients with renal insufficiency/failure and some elderly patients, because they are at risk for severe electrolyte imbalances. The phosphate or magnesium load results in hypokalemia, metabolic acidosis, and hypocalcemia.29Tan J.J.Y. Tjandra J.J. Which is the optimal bowel preparation for OC: a meta-analysis.Colorectal Dis. 2006; 8: 247-258Crossref PubMed Scopus (173) Google Scholar, 31Beloosesky Y. Grinblat J. Weiss A. et al.Electrolyte disorders following oral sodium phosphate administration for bowel cleansing in elderly patients.Arch Intern Med. 2003; 163: 803-808Crossref PubMed Scopus (163) Google Scholar, 32Fass R. Do S. Hixson L.J. Fatal hyperphosphatemia following Fleet Phospo-Soda in a patient with colonic ileus.Am J Gastroenterol. 1993; 88: 929-932PubMed Google Scholar, 33Fine A. Patterson J. Severe hyperphosphatemia following phosphate administration for bowel preparation in patients with renal failure: two cases and a review of the literature.Am J Kidney Dis. 1997; 29: 103-105Abstract Full Text PDF PubMed Scopus (99) Google Scholar, 34Lieberman D.A. Ghormley J. Flora K. Effect of oral sodium phosphate colon preparation on serum electrolytes in patients with normal serum creatinine.Gastrointest Endosc. 1996; 43: 467-469Abstract Full Text Full Text PDF PubMed Scopus (102) Google Scholar Mortality is increased, reported as high as 33% in those developing hyperphosphatemia after phosphate preparation,33Fine A. Patterson J. Severe hyperphosphatemia following phosphate administration for bowel preparation in patients with renal failure: two cases and a review of the literature.Am J Kidney Dis. 1997; 29: 103-105Abstract Full Text PDF PubMed Scopus (99) Google Scholar although the cause of death is unclear. Another completion enema quality issue is due to retention of gas after endoscopy, potentially decreasing the quality of DCBE. However, in a randomized control clinical trial,35Marshall J.B. Hoyt T.S. Seger R.M. et al.Air-contrast barium enema studies after flexible proctosigmoidoscopy: randomized controlled clinical trial.Radiology. 1990; 176: 549-551PubMed Google Scholar this was shown not to be the case, and the quality of the DCBE was not affected by performance of flexible proctosigmoidoscopy with room air or carbon dioxide. A potential confounding problem for the performance of DCBE after failed OC or for completion after flexible sigmoidoscopy is the risk of perforation if a mucosal biopsy or polypectomy has been performed. There is no consensus concerning the appropriate timing of DCBE after this. Most believe that DCBE can be safely performed on the same day in patients with superficial biopsy,36Harned R.K. Consigny P.M. Cooper N.B. et al.Barium enema examination following biopsy of the rectum or colon.Radiology. 1982; 145: 11-16PubMed Google Scholar, 37Harned R.K. Williams S.M. Maglinte D.D.T. et al.Clinical application of in vitro studies for barium-enema examination following colorectal biopsy.Radiology. 1985; 154: 319-321PubMed Google Scholar, 38Maglinte D.D. Strong R.C. Strate R.W. et al.Barium enema after colorectal biopsies: experimental data.AJR. 1982; 139: 693-697Crossref PubMed Scopus (26) Google Scholar but it should be delayed for 5–7 days after deep biopsy (involving muscularis propria) or polypectomy.36Harned R.K. Consigny P.M. Cooper N.B. et al.Barium enema examination following biopsy of the rectum or colon.Radiology. 1982; 145: 11-16PubMed Google Scholar, 37Harned R.K. Williams S.M. Maglinte D.D.T. et al.Clinical application of in vitro studies for barium-enema examination following colorectal biopsy.Radiology. 1985; 154: 319-321PubMed Google Scholar, 38Maglinte D.D. Strong R.C. Strate R.W. et al.Barium enema after colorectal biopsies: experimental data.AJR. 1982; 139: 693-697Crossref PubMed Scopus (26) Google Scholar, 39Low V.H. What is the current recommended waiting time for performance of a gastrointestinal barium study after endoscopic biopsy of the upper or lower gastrointestinal tract?.AJR. 1998; 170: 1104-1105Crossref PubMed Scopus (2) Google Scholar In one animal study, re-epithelialization of deep biopsies occurred within 6 days.38Maglinte D.D. Strong R.C. Strate R.W. et al.Barium enema after colorectal biopsies: experimental data.AJR. 1982; 139: 693-697Crossref PubMed Scopus (26) Google Scholar In a 4-pronged study, Harned et al36Harned R.K. Consigny P.M. Cooper N.B. et al.Barium enema examination following biopsy of the rectum or colon.Radiology. 1982; 145: 11-16PubMed Google Scholar surveyed 68 gastrointestinal radiologists, performed an in vitro study of pig colons post biopsy, measured colon pressure in human subjects, and performed a histologic analysis of human biopsy specimen. They concluded that superficial biopsy performed with a small colonic biopsy forceps does not require a waiting period before performance of DCBE, and biopsy with proctoscopic forceps should result in a waiting period of at least 7 days because these tend to be deeper biopsies extending to the muscularis propria. Therefore, the radiologist must know what type of biopsy has been performed before the enema examination, so appropriate decisions can be made about the timing. Regardless of all of these issues, the completion DCBE will too go to the wayside, replaced by same-day CTC. However, there have been continued delays in widespread implementation of CTC screening programs. There is little to no reimbursement in many states for this examination, and until this happens, DCBE will remain the mainstay for evaluation of patients after incomplete OC. Barium enema examination has a role in the preoperative patient with colorectal cancer. Although colorectal carcinoma is most often definitively diagnosed with colonoscopic visualization and biopsy, tumor localization can be difficult. DCBE is a quick examination that can localize cancers for surgical planning.40Frager D.H. Frager J.D. Wolf E.L. et al.Problems in the colonoscopic localization of tumors: continued value of the barium enema.Gastrointest Radiol. 1987; 12: 343-346Crossref PubMed Scopus (42) Google Scholar In addition, it can also evaluate the more proximal colon in patients with a nearly obstructing tumor that precludes colonoscopic visualization. The radiologist must take caution in not infusing a large quantity of barium proximal to these lumen-limiting, to prevent inspissation and so that an adequate bowel preparation can be obtained before colectomy. Again, the emerging application of CTC in this setting is promising41Fenlon H.M. McAneny D.B. Nunes D.P. et al.Occlusive colon carcinoma: virtual OC in the preoperative evaluation of the proximal colon.Radiology. 1999; 210: 423-428Crossref PubMed Scopus (239) Google Scholar, 42Morrin M.M. Farrell R.J. Raptopoulos V. et al.Role of virtual computed tomographic colonography in patients with colorectal cancers and obstructing colorectal lesions.Dis Colon Rectum. 2000; 43: 303-311Crossref PubMed Scopus (126) Google Scholar and will likely replace DCBE. Contrast enema examinations are valuable in the setting of pseudo-obstruction when cross-sectional imaging examinations are equivocal, ie, colonic distention with a discrete transition point but no identifiable obstructing mass or stricture.43Gilchrist A.M. Mills J.O. Russell C.G. Acute large-bowel pseudo-obstruction.Clin Radiol. 1985; 36: 401-404Abstract Full Text PDF PubMed Scopus (23) Google Scholar, 44Stewart J. Finan P.J. Courtney D.F. et al.Does a water soluble contrast enema assist in the management of acute large bowel obstruction: a prospective study of 117 cases.Br J Surg. 1984; 71: 799-801Crossref PubMed Scopus (51) Google Scholar It is a relatively simple and quick examination that can potentially prevent unnecessary OC and surgery. Because these patients are unprepped, water-soluble contrast is used to avoid inspissation of the barium agent. Many use this examination in a therapeutic manner for those with fecal impaction, although performance of the fluoroscopic portion of the examination is probably unnecessary in this population of patients. DCBE is still used in a variety of disease states, including diagnosis and evaluation of inflammatory bowel disease, constipation, and nonspecific abdominal pain. However, its role for these indications is declining. Some might argue that DCBE is a study of the past. Although this might be true in certain clinical scenarios, there is an important role for water-soluble enema examination in the postoperative patient, including those having undergone partial or total colectomy with low anterior resection and primary anastomosis or pouch reconstruction (Figure 2). It is the gold standard for the evaluation of anastomotic leak (Figure 3).45Dolinsky D. Levine M.S. Rubesin S.E. et al.Utility of contrast enema for detecting anastomotic strictures after total proctocolectomy and ileal pouch-anal anastomosis.AJR. 2007; 189: 25-29Crossref PubMed Scopus (26) Google Scholar, 46Hrung J.M. Levine M.S. Rombeau J.L. et al.Total proctocolectomy and ileoanal pouch: the role of contrast studies for evaluating postoperative leaks.Abdom Imaging. 1988; 23: 375-379Crossref Scopus (29) Google Scholar, 47Seggerman R.E. Chen M.Y. Waters G.S. et al.Radiology of ileal pouch-anal anastomosis surgery.AJR. 2003; 180: 999-1002Crossref PubMed Scopus (24) Google Scholar, 48Severini A. Civelli E.M. Uslenghi E. et al.Diagnostic and interventional radiology in the post-operative period and follow-up of patients after rectal resection with coloanal anastomosis.Eur Radiol. 2000; 10: 1101-1105Crossref PubMed Scopus (8) Google Scholar Although CT can diagnose abscess and contrast extravasation, fluoroscopy can identify the exact origin of the leak and even quantify the extent and interval improvement. This type of examination is a single-contrast study, so evaluation of mucosal detail is not possible, and it is not indicated in this scenario. It is a relatively quick procedure and can be performed in the obtunded patient. This type of contrast enema examination evaluates anastomotic integrity; therefore, water-soluble (iodine-based) contrast is indicated, because there is a risk of contrast spillage into the peritoneal cavity and its associated complications. Patients with a significant history of intravenous contrast allergy should not undergo water-soluble enema examination because small quantities of contrast can be absorbed across the mucosa of the colon into the bloodstream, particularly inflamed mucosa. Severe contrast reactions have been reported with intravenous contrast injection volumes as little as 1 mL. Therefore, studies in these patients should be avoided. Alternative diagnostic examinations include a non-contrast CT to identify abscess or a barium enema examination, although not ideal because of the risk of barium leakage. Barium incites a granulomatous reaction and subsequent adhesions, which is significantly increased when contaminated with fecal material. However, if the patient cannot be adequately evaluated by other means, this might be the only option.Figure 3A 25-year-old man, post total proctocolectomy with ileal pouch and ileoanal anastomosis for ulcerative colitis undergoing water-soluble contrast examination (pouchogram). Anastomosis (arrows) is widely patent, but there is a leak (curved arrows) extending from the anastomosis on the left.View Large Image Figure ViewerDownload Hi-res image Download (PPT) The role of the contrast enema examination is definitely evolving. Many of the traditional indications for these studies will soon be replaced by CTC. However, until then, the completion DCBE will continue to be performed at most institutions. The efficacy of CT is quickly being established, but its widespread application is limited for now by reimbursement issues. Hopefully, this will change in the near future. Regardless, there will always be a role for fluoroscopic contrast evaluation of the colon in postoperative patients and those with pseudo-obstruction. It is an accurate and quick examination that is low in cost and readily performed in most radiology departments.