- Email: [email protected]
Comparative Evaluation of the Fecal-Tagging Quality in CT Colonography
Comparative Evaluation of the Fecal-Tagging Quality in CT Colonography: Barium vs. Iodinated Oral Contrast Agent1 Koichi Nagata, MD, PhD, Anand Kumar Singh, MD, Minal Jagtiani Sangwaiya, MBBS, MRCS, MD, Janne Na¨ppi, PhD, Michael E. Zalis, MD, Wenli Cai, PhD, Hiroyuki Yoshida, PhD
Rationale and Objectives. The purpose of this evaluation was to compare the tagging quality of a barium-based regimen with that of iodine-based regimens for computed tomographic (CT) colonography. Materials and Methods. Tagging quality was assessed retrospectively in three different types of fecal-tagging CT colonographic cases: 24 barium-based cases, 22 nonionic iodine-based cases, and 24 ionic iodine-based cases. For the purpose of evaluation, the large intestine was divided into six segments, and the tagging homogeneity of a total of 420 segments (70 patients) was graded by three blinded readers from 0 (heterogeneous) to 4 (homogeneous). Results. For barium-based cases, the average score for the three readers was 2.4, whereas it was 3.4 for nonionic iodine and 3.6 for ionic iodine. The percentages of segments that were assigned scores of 4 (excellent tagging [100%]) were 11.6%, 61.9%, and 72.9% for the barium-based, nonionic iodine-based, and ionic iodine-based regimens, respectively. The homogeneity scores of iodine-based fecal-tagging regimens were significantly higher than those of the barium-based fecal-tagging regimen (P < .001). The CT attenuation values of tagging in the cases were also assessed: the minimum and maximum values were significantly higher for the iodine-based regimens than for the barium-based regimen (P < .001). Conclusions. The iodine-based fecal-tagging regimens provide significantly greater homogeneity in oral-tagging fecal material than the barium-based fecal-tagging regimen. Iodine-based fecal-tagging regimens can provide an appropriate method for use in nonlaxative or minimum-laxative CT colonography. Key Words. Computed tomography; virtual colonoscopy; tagging; iodinated contrast; barium. ª AUR, 2009
Thorough bowel cleansing and adequate distension are necessary for successful computed tomographic (CT) colonographic (CTC) examinations. However, patients often perceive these two procedures as the most unpleasant aspects of CTC examinations (1–3). Fecal tagging by orally administered positive-contrast agents can be used for the effective differentiation of fecal material from polyps by enhancing Acad Radiol 2009; 16:1393–1399 1 From the 3D Imaging Laboratory (K.N., A.K.S., J.N., W.C., H.Y.) and the Division of Abdominal Imaging and Interventional Radiology (M.J.S., M.E.Z.), Department of Radiology, Massachusetts General Hospital and Harvard Medical School, 25 New Chardon Street, Suite 400C, Boston, MA 02114 Dr Zalis received a research grant from GE (Milwaukee, WI). Address correspondence to: K.N. e-mail: [email protected]
ª AUR, 2009 doi:10.1016/j.acra.2009.05.003
residual stool and fluid, thus increasing the specificity of polyps (4–9). For distinguishing tagged fecal contents reliably from soft tissue lesions in the large intestine, the tagging of fecal material should be homogeneous (10,11). In general, three contrast agents are suitable for fecal-tagging CT colonography: barium sulfate, ionic iodine, and nonionic iodine (11–20). However, to our knowledge, the quality of tagging using these three contrast agents has never been compared in fecal-tagging CT colonography. In this study, we retrospectively compared the quality of tagging using three contrast agents with either nonlaxative or minimum-laxative regimens. The quality of tagging was assessed in terms of homogeneity and CT attenuation values (in Hounsfield units [HU]) of the residual fecal material. We also evaluated the observed presence of residual stool and fluid for each regimen.
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MATERIALS AND METHODS Study Group The cases of 70 patients who underwent CT colonography, including 36 women and 34 men with a mean age of 61 years, were collected at the Massachusetts General Hospital (Boston, MA) and Sakakibara Sapia Tower Clinic (Chiyodaku, Tokyo, Japan). The institutional review board of the Massachusetts General Hospital approved the procedures for the barium-based fecal-tagging CTC group and the nonionic iodine-based fecal-tagging CTC group. Full ethics committee approval was obtained at the Sakakibara Sapia Tower Clinic for the ionic iodine-based fecal-tagging CTC group. Patients were excluded from the study if they (1) were pregnant, (2) had conditions that are contraindications to the ingestion of contrast agents, (3) did not provide written informed consent or were unable to understand the concepts of patient information and informed consent, or (4) were aged <20 years. Twenty-four consecutive patients were examined from the barium group (11). The mean age was 61 years (range, 51–74 years). There were 10 women (42%) and 14 men (58%). Twenty-two consecutive patients were examined from the nonionic iodine group. The mean age was 60 years (range, 51–68 years), with 12 women (55%) and 10 men (45%). Twenty-four consecutive patients were examined from the ionic iodine group. The mean age was 62 years (range, 40–81 years), with 14 women (58%) and 10 men (42%). Fecal-Tagging Regimens In the barium group (11), patients ingested seven 150-mL aliquots of 2% barium sulfate suspension (E-Z-Cat; Bracco Diagnostics, Princeton, NJ) with each meal and snack for 48hours prior to CT scanning. A final 700-mL bolus of the same 2% barium sulfate suspension was ingested on the morning of the CT scan, 3hours prior to imaging. There were no food or fluid restrictions for patients. In the nonionic iodine group (11), patients ingested a nonionic iodinated contrast agent (Omnipaque 300; GE Healthcare, Waukesha, WI) with a concentration of 300mg of organically bound iodine per milliliter. Patients ingested the contrast agent in seven 10-mL aliquots with meals and snacks for 48hours prior to CT scanning, also without diet modification. Three hours prior to CT scanning, patients ingested a bolus of 30mL of nonionic iodinated contrast medium diluted in 700mL of water. In the ionic iodine group (21), patients followed a modified original dry preparation (6) by adding a small amount of sodium picosulfate as follows: 3 days prior to CT scanning, patients were asked to avoid fiber-rich food. There were no additional food or fluid restrictions for patients. After each meal, the patients were required to drink 5mL of ionic iodinated contrast medium (Gastrografin Oral; Bayer Yakuhin,
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Osaka, Japan) diluted in a standard glass of water for fecal tagging. Patients received a total of 45mL of the ionic iodinated contrast agent over the 3-day period preceding the CT scan and 10mL of sodium picosulfate solution (Laxoberon Solution; Teijin Pharma, Tokyo, Japan) for minimum laxative cleansing on the night prior to the scan.
CT Colonography Patients were placed on the CT table, and a flexible rubber catheter was inserted into the rectum. For distension of the colon, either air (barium and nonionic iodine groups) or carbon dioxide (ionic iodine group) was insufflated manually to maximum patient tolerance. A CT scout image was used to check the adequacy of the colorectal distension prior to the CTC study. Additional air or carbon dioxide was insufflated if needed. The CTC studies were performed in patients in the barium and nonionic iodine groups using a 4-detector-row CT system (LightSpeed; GE Medical Systems, Milwaukee, WI). The CT technique consisted of 3.75-mm collimation, a 1.8-mm reconstruction interval, a tube current–time product of 50mAs, and a tube voltage of 140 kVp. The CTC studies were performed in patients in the ionic iodine group with a 64-detector-row CT system (Aquilion 64; Toshiba Medical Systems, Otawara, Japan). The CT technique consisted of 0.5-mm collimation, a 0.5-mm reconstruction interval, automatic exposure control systems (VolumeEC; Toshiba Medical Systems, Otawara, Japan; minimum and maximum tube current, 10 and 500mA), and a tube voltage of 120 kVp. Antispasmodic agents, intravenous contrast, and sedation were not administered to any of the patients.
Evaluation of Residual Stool and Fluid and Tagging Quality An unblinded researcher randomly ordered the cases of the 70 CTC examinations. For evaluation, the large intestine was divided into six segments: (1) rectum, (2) sigmoid colon, (3) descending colon, (4) transverse colon, (5) ascending colon, and (6) cecum. Three blinded experienced physicians independently evaluated the CTC studies of the 70 patients using a CTC workstation (Rendoscopy Visualization version 2.0.15.3; Rendoscopy AG, Munich, Germany). All information about patients, scan dates, and scan parameters was anonymized. The type of fecal-tagging regimen was not disclosed to the three readers. The readers graded each case on the basis of axial images. Standard window settings were applied (window width, 1250 HU; window level, 50 HU), but the readers were permitted to adjust these settings. Electronic cleansing software was not used, and routine endoluminal fly-through was not performed for these evaluations. A total of 420 segments were scored in this manner in terms of the quality of preparation and tagging. At grading, readers
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Figure 1. Examples of the scoring of the presence of residual stool and fluid and their tagging quality. (a) In the transverse colon (circle), residual stool and fluid were scored 3 (large stool) and 0 (no fluid), respectively. Tagging homogeneity was scored 1 (poor tagging) by two of three readers. In the descending colon (arrow), residual stool and fluid were scored 3 and 0, respectively. Tagging homogeneity was scored 2 (inhomogeneous tagging) by two of three readers. (b) In the cecum (circle), sigmoid colon (arrow), and rectum (broken arrow), residual stool were scored 3 (large stool), 3, and 2 (moderate-size stool), respectively. Scores for residual fluid were all 0 (no fluid). Tagging homogeneities were all scored 4 (excellent tagging) by all three readers.
were suggested to reference an example case that represented each score for standardization of the scoring process. The observed amount of residual solid stool regardless of tagging was assessed on axial images using a 4-point scale: 0=no stool, 1=small stool (maximum diameter<6mm), 2 = moderate-size stool (6–9mm), and 3 = large stool ($10mm) (Fig 1). For each colorectal segment, the axial image with the largest residual stool was assessed, and the maximum diameter of the stool was measured in the axial cut-plane image using electronic calipers. The observed presence of residual fluid (regardless of tagging) was assessed on axial images using a 4-point scale: 0=no fluid, 1=minimal fluid (depth or width<6mm), 2 = moderate fluid (depth or width$6mm, depth<50% of the luminal circumference), and 3 = substantial fluid (depth$50% of the luminal circumference) (Fig 1). For each colorectal segment, the axial image with most residual fluid was reviewed, and the extent of fluid was measured in the axial cut-plane image using electronic calipers. The homogeneity of fecal tagging was assessed using a 5point scale: 0=no tagging (tagging<25%), 1 = poor tagging (25% # tagging<50%), 2 = inhomogeneous tagging (50% # tagging<75%), 3 = good tagging (75% # tagging<100%), and 4 = excellent tagging (100%) (Fig 1). The lowest score observed for fecal material within each segment was recorded. The CT attenuation values of tagged residual fluid or stool were measured manually by recording of the maximum and minimum attenuation values (in HU) in each segment. The maximum attenuation value was determined as the highest value in fecal regions of interest that a reader considered to have a bright white color. The minimum attenuation value was determined as the lowest value in fecal regions of interest
that a reader considered to have a relatively dark color. The CT attenuation values were not measured in segments with no observed fluid or stool. Statistical Analysis The measurement data were analyzed statistically using StatView version 5.0 (SAS Institute Inc, Cary, NC). We used Mann-Whitney U tests for the residual stool and fluid scores and the tagging homogeneity score, and Student’s t test was used for the minimum and maximum attenuation values. The results were considered statistically significant at P < .05. Interreader reliabilities were examined using intraclass correlation coefficients (ICCs) for the three independent readers. The agreement of the residual stool or fluid score and tagging quality among the readers was considered fair to good for ICCs of 0.4 to 0.75 and excellent for ICCs>0.75. An ICC of 0 indicates an absence of agreement, and negative k values indicate disagreement (22). RESULTS Bowel Preparation For the observed amount of residual stool, the percentages of segments that were assigned scores of 0 (no observed stool) were 3.2% for the barium group, 16.9% for the nonionic iodine group, and 30.6% for the ionic iodine group (Fig 2). The percentages of segments that were assigned scores of 3 (stool$10mm) were 82.9% for the barium group, 65.2% for the nonionic iodine group, and 51.4% for the ionic iodine group (Fig 2). The average scores of residual stool for all segments were 2.74 for the barium group, 2.26 for the nonionic iodine group, and 1.87 for the ionic iodine group. The differences observed between the residual-
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Figure 2. Percentages of the residual stool scores in all colon segments for the barium group, nonionic iodine group, and ionic iodine group. Scoring: 0=no stool, 1=small stool (maximum diameter<6mm), 2 = moderate-size stool (6–9mm), 3 = large stool ($10mm).
stool scores for each tagging regimen were significant: P=.0051 for the barium group compared to the nonionic iodine group, P=.022 for the nonionic iodine group compared to the ionic iodine group, and P < .001 for the barium group compared to the ionic iodine group. The scores of agreement between readers were tested using ICCs (22): the ICCs for reader 1 versus reader 2, reader 2 versus reader 3, and reader 1 versus reader 3 were 0.47, 0.61, and 0.58, respectively, indicating good agreement among all three readers. For residual fluid, the percentages of segments that were assigned scores of 0 (no fluid) were 96.1%, 72.5%, and 93.1% for the barium, nonionic iodine, and ionic iodine groups, respectively (Fig 3). The percentages of segments that were assigned scores of 3 (depth$50% of the luminal circumference) were 0.2%, 2.5%, and 0.0% for the barium, nonionic iodine, and ionic iodine groups, respectively (Fig 3). The average fluid scores in the segments were 0.07, 0.57, and 0.13 for the barium, nonionic iodine, and ionic iodine groups, respectively. Significant differences were observed for the residual fluid score and tagging regimens in the barium group compared to the nonionic iodine group (P=.0008) and for the nonionic iodine group compared to the ionic iodine group (P=.0029). However, no significant differences were observed in the fluid scores between the barium group and the ionic iodine group (P=.68). The scores of agreement by ICC for reader 1 versus reader 2, reader 2 versus reader 3, and reader 1 versus reader 3 were 0.72, 0.57, and 0.84, respectively, indicating good to excellent agreement. Tagging Quality The average tagging homogeneity scores assigned by the three readers for all segments in the barium group were 2.2,
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Figure 3. Percentages of the residual fluid scores in all colon segments for the barium group, nonionic iodine group, and ionic iodine group. Scoring: 0=no fluid, 1=minimal fluid (depth or width<6mm), 2 = moderate fluid (depth or width$6mm, depth<50% of the luminal circumference), and 3 = substantial fluid (depth$50% of the luminal circumference).
2.4, and 2.7. The scores for the iodine groups were higher: for the nonionic iodine group, they were 3.3, 3.3, and 3.6, and for the ionic iodine group, they were 3.6, 3.5, and 3.8 (Fig 4). The percentages of segments that were assigned scores of 4 (excellent tagging [100%]) were 11.6%, 61.9%, and 72.9% for the barium, nonionic iodine, and ionic iodine groups, respectively. The tagging homogeneity scores of the barium group were significantly different from the scores of the ionic and nonionic iodine groups (P < .001). Also, the tagging homogeneity of the nonionic iodine group and ionic iodine group differed significantly (P=.0021). The scores of agreement by ICC for reader 1 versus reader 2, reader 2 versus reader 3, and reader 1 versus reader 3 were 0.74, 0.69, and 0.76, respectively, indicating good to excellent agreement. The average maximum attenuation values obtained by the three readers for all segments in the barium group were 500, 410, and 465 HU. In contrast, the scores for the nonionic iodine group were 706, 670, and 635 HU, and for the ionic iodine group, they were 663, 657, and 601 HU, respectively (Fig 5). The average minimum attenuation values obtained by the three readers for all segments in the barium group were 53, 146, and 186 HU. In contrast, the scores for the nonionic iodine group were 353, 414, and 458 HU, and for the ionic iodine group, they were 405, 352, and 482 HU (Fig 6). The minimum and maximum attenuation values for the barium group were significantly lower than those for the ionic and nonionic iodine groups (P < .001). However, no significant differences were seen in the maximum attenuation values (P < .098) and minimum attenuation values (P < .69) between the nonionic iodine group and the ionic iodine group.
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Figure 4. Tagging homogeneity scores of each reader and the average tagging homogeneity scores for the barium group, nonionic iodine group, and ionic iodine group. Distal colon=rectum, sigmoid colon, and descending colon. Proximal colon=transverse colon, ascending colon, and cecum. Scoring: 0=no tagging (tagging<25%), 1 = poor tagging (25% # tagging<50%), 2 = inhomogeneous tagging (50% # tagging<75%), 3 = good tagging (75% # tagging<100%), and 4 = excellent tagging (100%).
Figure 5. Maximum attenuation values of each reader and the average maximum attenuation values for the barium group, nonionic iodine group, and ionic iodine group. Distal colon=rectum, sigmoid colon, and descending colon. Proximal colon=transverse colon, ascending colon, and cecum. HU, Hounsfield units.
DISCUSSION In state-of-the-art CT colonography, orally administered positive-contrast tagging agents are used routinely for the labeling of residual feces (23,24). At present, there are many potential candidates for the implementation of fecal-tagging
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Figure 6. Minimum attenuation values of each reader and the average minimum attenuation values for the barium group, nonionic iodine group, and ionic iodine group. Distal colon=rectum, sigmoid colon, and descending colon. Proximal colon=transverse colon, ascending colon, and cecum. HU, Hounsfield units.
regimens for CTC studies. Ideally, fecal tagging for CT colonography should be safe, have high quality, and be cost effective, well tolerated, and easy to perform. Unfortunately, there is no consensus on such a regimen. However, three types of oral-tagging contrast agents are used in most fecaltagging regimens: barium sulfate suspension, nonionic iodinated contrast medium, and ionic iodinated contrast medium. In this study, we considered three available fecaltagging CTC regimens that represented each tagging agent. Combinations of tagging agents were not considered, because the use of only one contrast agent may simplify bowel preparation for patients. The European Society of Gastrointestinal and Abdominal Radiology emphasizes that the choice of oral-tagging contrast agents should be based on local experience, with due regard given to any history of allergy (23). Some investigators prefer barium sulfate for fecal tagging because it is safe, it is not absorbed by the gastrointestinal tract, and it is inexpensive (17,18,25). However, barium sometimes produces a mix of tagging densities in one fluid level, with low-attenuation feces located above high-density barium, which can result in a beam-hardening artifact on computed tomography (14,17,26). Our study showed that barium produces less homogeneous tagging than ionic or nonionic iodinated contrast (both P values < .05). The attenuation values for the barium group were significantly lower than those for the nonionic iodinated group and the ionic iodinated group (both P values < .05). In addition, barium can cause constipation or even impaction (27). For CT imaging, the American College of Radiology recommends the use of water-soluble contrast agents over barium in some
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specific clinical situations, such as suspected gastrointestinal perforation and administration before bowel surgery (28). Nonionic iodinated contrast is water soluble and has low viscosity, allowing uniform distribution. It can be used safely in cases of gastrointestinal tract perforation because it is rapidly absorbed (29). It has a low risk for causing dehydration and diarrhea. In addition, it is almost tasteless and has good patient acceptance (30,31). Studies of the usefulness of nonionic iodinated contrast compared with barium as an oral agent have been reported (11,31,32). However, this contrast agent is more expensive than both barium and ionic iodinated contrast. Similar to nonionic iodinated contrast, ionic iodinated contrast is also water soluble and is considered safe when patients with suspected bowel perforation are examined. It is less expensive than nonionic iodinated contrast. The oral administration of this contrast agent is widely used for abdominal and pelvic CT scans (27). However, many patients do not like the taste of ionic iodinated contrast medium when drinking large amounts (33). In addition, high-osmolar contrast agents can cause gastrointestinal complaints (eg, nausea, vomiting, cramps, diarrhea), especially at high concentrations. In consideration of these factors, small quantities of ionic iodinated contrast were used in this study (a total of 45mL over 3 days). These quantities proved adequate for fecal tagging. The iodine-based fecal-tagging regimen provided significantly greater homogeneity in tagging fecal material than the barium-based fecal-tagging regimen. For this reason, the iodinated oral contrast agent may result in fewer electronic cleansing artifacts (11). Because iodinated contrast medium is water soluble, it permits excellent tagging homogeneity not only for residual fluid but also for residual stool (6,8,11,21). Ionic iodine-based fecal-tagging CTC studies with minimum laxative cleansing had homogeneity superior to that of nonionic iodine-based fecal-tagging CTC studies without laxative cleansing. Small quantities (10mL) of sodium picosulfate solution were used in the ionic iodine group. However, a nonionic iodine group with minimum laxative cleansing may achieve similar results. As expected, the ionic iodine-based fecal-tagging regimen with minimum laxative resulted in significantly better quality bowel preparation than the two nonlaxative regimens (the barium and nonionic iodine groups). This result might also have been due to the washing effect of the ionic iodine-based contrast agent (11). More stools were found in the barium and nonionic iodine groups than in the ionic iodine group (both P values < .05). More fluid was found in the nonionic iodine group than in the ionic iodine group (P < .05). It was unexpected that there were quality differences in bowel preparation between the two nonlaxative regimens. More stools were found in the barium group than in the nonionic iodine group (P < .05). In contrast, more fluid was found in the nonionic
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iodine group than in the barium group (P < .05). Overall, there were more residual stools or fluid in the nonlaxative regimens than in the minimum-laxative regimen. Dachman et al (34) found that nonlaxative regimens that left significant residual feces, even if well tagged, were not desirable, because greater quantities of feces made the examinations more difficult to interpret. This study was limited in that it was not a prospective study. The bowel preparation (nonlaxative or minimumlaxative, total dose of contrast agents, and duration of preparation) and the scanning protocols were heterogeneous. The use of different CT scanners from different manufactures and slightly different CT parameters, such as the use or not of automatic tube current modulation (35), may have affect the measurements of CT attenuation; however, the CT scanners are regularity calibrated, and thus this effect is predictable and expected to be small. A second limitation is that we did not evaluate the accuracy of colorectal polyp detection, because the limited number of true-positive cases made this impractical. However, our purpose in this study was to evaluate homogeneity for each oral-tagging contrast agent. The results of our study may provide a basis for future assessments of fecal-tagging regimens for CT colonography. Third, we did not evaluate the patients’ acceptance or discomfort regarding the bowel preparation procedure. In conclusion, the iodine-based fecal-tagging regimens provided significantly greater homogeneity in the oral tagging of fecal material than the barium-based fecal-tagging regimen. Iodine-based regimens can provide an appropriate fecal-tagging method for nonlaxative or minimum-laxative CTC studies.
ACKNOWLEDGMENTS
We thank Tomoko Imasawa, MD, Tomoko Obunai, MD, Atsushi Iyama, RT, and Teppei Mikami, RT, for their technical cooperation and Ms Elisabeth Lanzl for assistance in editing this report.
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21. Nagata K, Okawa T, Honma A, Endo S, Kudo S, Yoshida H. Full-laxative vs. minimum-laxative fecal-tagging CT colonography using 64-detectorrow CT: prospective blinded comparison of diagnostic performance, tagging quality, and patient acceptance. Acad Radiol 2009; 16:780–789. 22. Ross B. Fundamentals of biostatistics. New York: Duxbury Press, 1995. 23. Taylor SA, Laghi A, Lefere P, Halligan S, Stoker J. European Society of Gastrointestinal and Abdominal Radiology (ESGAR): consensus statement on CT colonography. Eur Radiol 2007; 17:575–579. 24. Nagata K, Na¨ppi J, Cai W, Yoshida H. Minimum-invasive early diagnosis of colorectal cancer with CT colonography: techniques and clinical value. Expert Opin Med Diagn 2008; 2:1233–1246. 25. Johnson KT, Carston MJ, Wentz RJ, Manduca A, Anderson SM, Johnson CD. Development of a cathartic-free colorectal cancer screening test using virtual colonoscopy: a feasibility study. AJR Am J Roentgenol 2007; 188:W29–W36. 26. Langer R, Kaufmann HJ. Nonionic contrast media for gastro-intestinal studies in newborns and infants. J Belge Radiol 1987; 70:211–216. 27. Horton KM, Fishman EK, Gayler B. The use of iohexol as oral contrast for computed tomography of the abdomen and pelvis. J Comput Assist Tomogr 2008; 32:207–209. 28. American College of Radiology. Manual on contrast media: version 6: 2008. Available at: http://www.scribd.com/doc/2952016/ Contrast-Media-Administration-Guidelines-by-the-ACR-American -College-of-Radiology-Version-6-2008. Accessed February 9, 2009. 29. Laerum F, Stordahl A, Solheim KE, Haugstvedt JR, Roald HE, Skinningsrud K. Intestinal follow-through examinations with iohexol and iopentol. Permeability alterations and efficacy in patients with small bowel obstruction. Invest Radiol 1991; 26(suppl):S177–S181. 30. Lonnemark M, Magnusson A. Oral contrast media in CT of the abdomen. Iohexol of different concentrations as a gastrointestinal contrast medium. Acta Radiol 1995; 36:396–398. 31. Stordahl A, Laerum F, Gjolberg T, Enge I. Water-soluble contrast media in radiography of small bowel obstruction. Comparison of ionic and nonionic contrast media. Acta Radiol 1988; 29:53–56. 32. Cohen MD, Towbin R, Baker S, et al. Comparison of iohexol with barium in gastrointestinal studies of infants and children. AJR Am J Roentgenol 1991; 156:345–350. 33. Diederichs G, Franiel T, Asbach P, Romano V, Hamm B, Rogalla P. Oral administration of intravenous contrast media: a tasty alternative to conventional oral contrast media in computed tomography. Rofo 2007; 179: 1061–1067. 34. Dachman AH, Dawson DO, Lefere P, et al. Comparison of routine and unprepped CT colonography augmented by low fiber diet and stool tagging: a pilot study. Abdom Imaging 2007; 32:96–104. 35. Kalra MK, Maher MM, Toth TL, et al. Techniques and applications of automatic tube current modulation for CT. Radiology 2004; 233:649–657.
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Rationale and Objectives. The purpose of this evaluation was to compare the tagging quality of a barium-based regimen with that of iodine-based regimens for computed tomographic (CT) colonography. Materials and Methods. Tagging quality was assessed retrospectively in three different types of fecal-tagging CT colonographic cases: 24 barium-based cases, 22 nonionic iodine-based cases, and 24 ionic iodine-based cases. For the purpose of evaluation, the large intestine was divided into six segments, and the tagging homogeneity of a total of 420 segments (70 patients) was graded by three blinded readers from 0 (heterogeneous) to 4 (homogeneous). Results. For barium-based cases, the average score for the three readers was 2.4, whereas it was 3.4 for nonionic iodine and 3.6 for ionic iodine. The percentages of segments that were assigned scores of 4 (excellent tagging [100%]) were 11.6%, 61.9%, and 72.9% for the barium-based, nonionic iodine-based, and ionic iodine-based regimens, respectively. The homogeneity scores of iodine-based fecal-tagging regimens were significantly higher than those of the barium-based fecal-tagging regimen (P < .001). The CT attenuation values of tagging in the cases were also assessed: the minimum and maximum values were significantly higher for the iodine-based regimens than for the barium-based regimen (P < .001). Conclusions. The iodine-based fecal-tagging regimens provide significantly greater homogeneity in oral-tagging fecal material than the barium-based fecal-tagging regimen. Iodine-based fecal-tagging regimens can provide an appropriate method for use in nonlaxative or minimum-laxative CT colonography. Key Words. Computed tomography; virtual colonoscopy; tagging; iodinated contrast; barium. ª AUR, 2009
Thorough bowel cleansing and adequate distension are necessary for successful computed tomographic (CT) colonographic (CTC) examinations. However, patients often perceive these two procedures as the most unpleasant aspects of CTC examinations (1–3). Fecal tagging by orally administered positive-contrast agents can be used for the effective differentiation of fecal material from polyps by enhancing Acad Radiol 2009; 16:1393–1399 1 From the 3D Imaging Laboratory (K.N., A.K.S., J.N., W.C., H.Y.) and the Division of Abdominal Imaging and Interventional Radiology (M.J.S., M.E.Z.), Department of Radiology, Massachusetts General Hospital and Harvard Medical School, 25 New Chardon Street, Suite 400C, Boston, MA 02114 Dr Zalis received a research grant from GE (Milwaukee, WI). Address correspondence to: K.N. e-mail: [email protected]
ª AUR, 2009 doi:10.1016/j.acra.2009.05.003
residual stool and fluid, thus increasing the specificity of polyps (4–9). For distinguishing tagged fecal contents reliably from soft tissue lesions in the large intestine, the tagging of fecal material should be homogeneous (10,11). In general, three contrast agents are suitable for fecal-tagging CT colonography: barium sulfate, ionic iodine, and nonionic iodine (11–20). However, to our knowledge, the quality of tagging using these three contrast agents has never been compared in fecal-tagging CT colonography. In this study, we retrospectively compared the quality of tagging using three contrast agents with either nonlaxative or minimum-laxative regimens. The quality of tagging was assessed in terms of homogeneity and CT attenuation values (in Hounsfield units [HU]) of the residual fecal material. We also evaluated the observed presence of residual stool and fluid for each regimen.
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MATERIALS AND METHODS Study Group The cases of 70 patients who underwent CT colonography, including 36 women and 34 men with a mean age of 61 years, were collected at the Massachusetts General Hospital (Boston, MA) and Sakakibara Sapia Tower Clinic (Chiyodaku, Tokyo, Japan). The institutional review board of the Massachusetts General Hospital approved the procedures for the barium-based fecal-tagging CTC group and the nonionic iodine-based fecal-tagging CTC group. Full ethics committee approval was obtained at the Sakakibara Sapia Tower Clinic for the ionic iodine-based fecal-tagging CTC group. Patients were excluded from the study if they (1) were pregnant, (2) had conditions that are contraindications to the ingestion of contrast agents, (3) did not provide written informed consent or were unable to understand the concepts of patient information and informed consent, or (4) were aged <20 years. Twenty-four consecutive patients were examined from the barium group (11). The mean age was 61 years (range, 51–74 years). There were 10 women (42%) and 14 men (58%). Twenty-two consecutive patients were examined from the nonionic iodine group. The mean age was 60 years (range, 51–68 years), with 12 women (55%) and 10 men (45%). Twenty-four consecutive patients were examined from the ionic iodine group. The mean age was 62 years (range, 40–81 years), with 14 women (58%) and 10 men (42%). Fecal-Tagging Regimens In the barium group (11), patients ingested seven 150-mL aliquots of 2% barium sulfate suspension (E-Z-Cat; Bracco Diagnostics, Princeton, NJ) with each meal and snack for 48hours prior to CT scanning. A final 700-mL bolus of the same 2% barium sulfate suspension was ingested on the morning of the CT scan, 3hours prior to imaging. There were no food or fluid restrictions for patients. In the nonionic iodine group (11), patients ingested a nonionic iodinated contrast agent (Omnipaque 300; GE Healthcare, Waukesha, WI) with a concentration of 300mg of organically bound iodine per milliliter. Patients ingested the contrast agent in seven 10-mL aliquots with meals and snacks for 48hours prior to CT scanning, also without diet modification. Three hours prior to CT scanning, patients ingested a bolus of 30mL of nonionic iodinated contrast medium diluted in 700mL of water. In the ionic iodine group (21), patients followed a modified original dry preparation (6) by adding a small amount of sodium picosulfate as follows: 3 days prior to CT scanning, patients were asked to avoid fiber-rich food. There were no additional food or fluid restrictions for patients. After each meal, the patients were required to drink 5mL of ionic iodinated contrast medium (Gastrografin Oral; Bayer Yakuhin,
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Osaka, Japan) diluted in a standard glass of water for fecal tagging. Patients received a total of 45mL of the ionic iodinated contrast agent over the 3-day period preceding the CT scan and 10mL of sodium picosulfate solution (Laxoberon Solution; Teijin Pharma, Tokyo, Japan) for minimum laxative cleansing on the night prior to the scan.
CT Colonography Patients were placed on the CT table, and a flexible rubber catheter was inserted into the rectum. For distension of the colon, either air (barium and nonionic iodine groups) or carbon dioxide (ionic iodine group) was insufflated manually to maximum patient tolerance. A CT scout image was used to check the adequacy of the colorectal distension prior to the CTC study. Additional air or carbon dioxide was insufflated if needed. The CTC studies were performed in patients in the barium and nonionic iodine groups using a 4-detector-row CT system (LightSpeed; GE Medical Systems, Milwaukee, WI). The CT technique consisted of 3.75-mm collimation, a 1.8-mm reconstruction interval, a tube current–time product of 50mAs, and a tube voltage of 140 kVp. The CTC studies were performed in patients in the ionic iodine group with a 64-detector-row CT system (Aquilion 64; Toshiba Medical Systems, Otawara, Japan). The CT technique consisted of 0.5-mm collimation, a 0.5-mm reconstruction interval, automatic exposure control systems (VolumeEC; Toshiba Medical Systems, Otawara, Japan; minimum and maximum tube current, 10 and 500mA), and a tube voltage of 120 kVp. Antispasmodic agents, intravenous contrast, and sedation were not administered to any of the patients.
Evaluation of Residual Stool and Fluid and Tagging Quality An unblinded researcher randomly ordered the cases of the 70 CTC examinations. For evaluation, the large intestine was divided into six segments: (1) rectum, (2) sigmoid colon, (3) descending colon, (4) transverse colon, (5) ascending colon, and (6) cecum. Three blinded experienced physicians independently evaluated the CTC studies of the 70 patients using a CTC workstation (Rendoscopy Visualization version 2.0.15.3; Rendoscopy AG, Munich, Germany). All information about patients, scan dates, and scan parameters was anonymized. The type of fecal-tagging regimen was not disclosed to the three readers. The readers graded each case on the basis of axial images. Standard window settings were applied (window width, 1250 HU; window level, 50 HU), but the readers were permitted to adjust these settings. Electronic cleansing software was not used, and routine endoluminal fly-through was not performed for these evaluations. A total of 420 segments were scored in this manner in terms of the quality of preparation and tagging. At grading, readers
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Figure 1. Examples of the scoring of the presence of residual stool and fluid and their tagging quality. (a) In the transverse colon (circle), residual stool and fluid were scored 3 (large stool) and 0 (no fluid), respectively. Tagging homogeneity was scored 1 (poor tagging) by two of three readers. In the descending colon (arrow), residual stool and fluid were scored 3 and 0, respectively. Tagging homogeneity was scored 2 (inhomogeneous tagging) by two of three readers. (b) In the cecum (circle), sigmoid colon (arrow), and rectum (broken arrow), residual stool were scored 3 (large stool), 3, and 2 (moderate-size stool), respectively. Scores for residual fluid were all 0 (no fluid). Tagging homogeneities were all scored 4 (excellent tagging) by all three readers.
were suggested to reference an example case that represented each score for standardization of the scoring process. The observed amount of residual solid stool regardless of tagging was assessed on axial images using a 4-point scale: 0=no stool, 1=small stool (maximum diameter<6mm), 2 = moderate-size stool (6–9mm), and 3 = large stool ($10mm) (Fig 1). For each colorectal segment, the axial image with the largest residual stool was assessed, and the maximum diameter of the stool was measured in the axial cut-plane image using electronic calipers. The observed presence of residual fluid (regardless of tagging) was assessed on axial images using a 4-point scale: 0=no fluid, 1=minimal fluid (depth or width<6mm), 2 = moderate fluid (depth or width$6mm, depth<50% of the luminal circumference), and 3 = substantial fluid (depth$50% of the luminal circumference) (Fig 1). For each colorectal segment, the axial image with most residual fluid was reviewed, and the extent of fluid was measured in the axial cut-plane image using electronic calipers. The homogeneity of fecal tagging was assessed using a 5point scale: 0=no tagging (tagging<25%), 1 = poor tagging (25% # tagging<50%), 2 = inhomogeneous tagging (50% # tagging<75%), 3 = good tagging (75% # tagging<100%), and 4 = excellent tagging (100%) (Fig 1). The lowest score observed for fecal material within each segment was recorded. The CT attenuation values of tagged residual fluid or stool were measured manually by recording of the maximum and minimum attenuation values (in HU) in each segment. The maximum attenuation value was determined as the highest value in fecal regions of interest that a reader considered to have a bright white color. The minimum attenuation value was determined as the lowest value in fecal regions of interest
that a reader considered to have a relatively dark color. The CT attenuation values were not measured in segments with no observed fluid or stool. Statistical Analysis The measurement data were analyzed statistically using StatView version 5.0 (SAS Institute Inc, Cary, NC). We used Mann-Whitney U tests for the residual stool and fluid scores and the tagging homogeneity score, and Student’s t test was used for the minimum and maximum attenuation values. The results were considered statistically significant at P < .05. Interreader reliabilities were examined using intraclass correlation coefficients (ICCs) for the three independent readers. The agreement of the residual stool or fluid score and tagging quality among the readers was considered fair to good for ICCs of 0.4 to 0.75 and excellent for ICCs>0.75. An ICC of 0 indicates an absence of agreement, and negative k values indicate disagreement (22). RESULTS Bowel Preparation For the observed amount of residual stool, the percentages of segments that were assigned scores of 0 (no observed stool) were 3.2% for the barium group, 16.9% for the nonionic iodine group, and 30.6% for the ionic iodine group (Fig 2). The percentages of segments that were assigned scores of 3 (stool$10mm) were 82.9% for the barium group, 65.2% for the nonionic iodine group, and 51.4% for the ionic iodine group (Fig 2). The average scores of residual stool for all segments were 2.74 for the barium group, 2.26 for the nonionic iodine group, and 1.87 for the ionic iodine group. The differences observed between the residual-
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Figure 2. Percentages of the residual stool scores in all colon segments for the barium group, nonionic iodine group, and ionic iodine group. Scoring: 0=no stool, 1=small stool (maximum diameter<6mm), 2 = moderate-size stool (6–9mm), 3 = large stool ($10mm).
stool scores for each tagging regimen were significant: P=.0051 for the barium group compared to the nonionic iodine group, P=.022 for the nonionic iodine group compared to the ionic iodine group, and P < .001 for the barium group compared to the ionic iodine group. The scores of agreement between readers were tested using ICCs (22): the ICCs for reader 1 versus reader 2, reader 2 versus reader 3, and reader 1 versus reader 3 were 0.47, 0.61, and 0.58, respectively, indicating good agreement among all three readers. For residual fluid, the percentages of segments that were assigned scores of 0 (no fluid) were 96.1%, 72.5%, and 93.1% for the barium, nonionic iodine, and ionic iodine groups, respectively (Fig 3). The percentages of segments that were assigned scores of 3 (depth$50% of the luminal circumference) were 0.2%, 2.5%, and 0.0% for the barium, nonionic iodine, and ionic iodine groups, respectively (Fig 3). The average fluid scores in the segments were 0.07, 0.57, and 0.13 for the barium, nonionic iodine, and ionic iodine groups, respectively. Significant differences were observed for the residual fluid score and tagging regimens in the barium group compared to the nonionic iodine group (P=.0008) and for the nonionic iodine group compared to the ionic iodine group (P=.0029). However, no significant differences were observed in the fluid scores between the barium group and the ionic iodine group (P=.68). The scores of agreement by ICC for reader 1 versus reader 2, reader 2 versus reader 3, and reader 1 versus reader 3 were 0.72, 0.57, and 0.84, respectively, indicating good to excellent agreement. Tagging Quality The average tagging homogeneity scores assigned by the three readers for all segments in the barium group were 2.2,
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Figure 3. Percentages of the residual fluid scores in all colon segments for the barium group, nonionic iodine group, and ionic iodine group. Scoring: 0=no fluid, 1=minimal fluid (depth or width<6mm), 2 = moderate fluid (depth or width$6mm, depth<50% of the luminal circumference), and 3 = substantial fluid (depth$50% of the luminal circumference).
2.4, and 2.7. The scores for the iodine groups were higher: for the nonionic iodine group, they were 3.3, 3.3, and 3.6, and for the ionic iodine group, they were 3.6, 3.5, and 3.8 (Fig 4). The percentages of segments that were assigned scores of 4 (excellent tagging [100%]) were 11.6%, 61.9%, and 72.9% for the barium, nonionic iodine, and ionic iodine groups, respectively. The tagging homogeneity scores of the barium group were significantly different from the scores of the ionic and nonionic iodine groups (P < .001). Also, the tagging homogeneity of the nonionic iodine group and ionic iodine group differed significantly (P=.0021). The scores of agreement by ICC for reader 1 versus reader 2, reader 2 versus reader 3, and reader 1 versus reader 3 were 0.74, 0.69, and 0.76, respectively, indicating good to excellent agreement. The average maximum attenuation values obtained by the three readers for all segments in the barium group were 500, 410, and 465 HU. In contrast, the scores for the nonionic iodine group were 706, 670, and 635 HU, and for the ionic iodine group, they were 663, 657, and 601 HU, respectively (Fig 5). The average minimum attenuation values obtained by the three readers for all segments in the barium group were 53, 146, and 186 HU. In contrast, the scores for the nonionic iodine group were 353, 414, and 458 HU, and for the ionic iodine group, they were 405, 352, and 482 HU (Fig 6). The minimum and maximum attenuation values for the barium group were significantly lower than those for the ionic and nonionic iodine groups (P < .001). However, no significant differences were seen in the maximum attenuation values (P < .098) and minimum attenuation values (P < .69) between the nonionic iodine group and the ionic iodine group.
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Figure 4. Tagging homogeneity scores of each reader and the average tagging homogeneity scores for the barium group, nonionic iodine group, and ionic iodine group. Distal colon=rectum, sigmoid colon, and descending colon. Proximal colon=transverse colon, ascending colon, and cecum. Scoring: 0=no tagging (tagging<25%), 1 = poor tagging (25% # tagging<50%), 2 = inhomogeneous tagging (50% # tagging<75%), 3 = good tagging (75% # tagging<100%), and 4 = excellent tagging (100%).
Figure 5. Maximum attenuation values of each reader and the average maximum attenuation values for the barium group, nonionic iodine group, and ionic iodine group. Distal colon=rectum, sigmoid colon, and descending colon. Proximal colon=transverse colon, ascending colon, and cecum. HU, Hounsfield units.
DISCUSSION In state-of-the-art CT colonography, orally administered positive-contrast tagging agents are used routinely for the labeling of residual feces (23,24). At present, there are many potential candidates for the implementation of fecal-tagging
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Figure 6. Minimum attenuation values of each reader and the average minimum attenuation values for the barium group, nonionic iodine group, and ionic iodine group. Distal colon=rectum, sigmoid colon, and descending colon. Proximal colon=transverse colon, ascending colon, and cecum. HU, Hounsfield units.
regimens for CTC studies. Ideally, fecal tagging for CT colonography should be safe, have high quality, and be cost effective, well tolerated, and easy to perform. Unfortunately, there is no consensus on such a regimen. However, three types of oral-tagging contrast agents are used in most fecaltagging regimens: barium sulfate suspension, nonionic iodinated contrast medium, and ionic iodinated contrast medium. In this study, we considered three available fecaltagging CTC regimens that represented each tagging agent. Combinations of tagging agents were not considered, because the use of only one contrast agent may simplify bowel preparation for patients. The European Society of Gastrointestinal and Abdominal Radiology emphasizes that the choice of oral-tagging contrast agents should be based on local experience, with due regard given to any history of allergy (23). Some investigators prefer barium sulfate for fecal tagging because it is safe, it is not absorbed by the gastrointestinal tract, and it is inexpensive (17,18,25). However, barium sometimes produces a mix of tagging densities in one fluid level, with low-attenuation feces located above high-density barium, which can result in a beam-hardening artifact on computed tomography (14,17,26). Our study showed that barium produces less homogeneous tagging than ionic or nonionic iodinated contrast (both P values < .05). The attenuation values for the barium group were significantly lower than those for the nonionic iodinated group and the ionic iodinated group (both P values < .05). In addition, barium can cause constipation or even impaction (27). For CT imaging, the American College of Radiology recommends the use of water-soluble contrast agents over barium in some
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specific clinical situations, such as suspected gastrointestinal perforation and administration before bowel surgery (28). Nonionic iodinated contrast is water soluble and has low viscosity, allowing uniform distribution. It can be used safely in cases of gastrointestinal tract perforation because it is rapidly absorbed (29). It has a low risk for causing dehydration and diarrhea. In addition, it is almost tasteless and has good patient acceptance (30,31). Studies of the usefulness of nonionic iodinated contrast compared with barium as an oral agent have been reported (11,31,32). However, this contrast agent is more expensive than both barium and ionic iodinated contrast. Similar to nonionic iodinated contrast, ionic iodinated contrast is also water soluble and is considered safe when patients with suspected bowel perforation are examined. It is less expensive than nonionic iodinated contrast. The oral administration of this contrast agent is widely used for abdominal and pelvic CT scans (27). However, many patients do not like the taste of ionic iodinated contrast medium when drinking large amounts (33). In addition, high-osmolar contrast agents can cause gastrointestinal complaints (eg, nausea, vomiting, cramps, diarrhea), especially at high concentrations. In consideration of these factors, small quantities of ionic iodinated contrast were used in this study (a total of 45mL over 3 days). These quantities proved adequate for fecal tagging. The iodine-based fecal-tagging regimen provided significantly greater homogeneity in tagging fecal material than the barium-based fecal-tagging regimen. For this reason, the iodinated oral contrast agent may result in fewer electronic cleansing artifacts (11). Because iodinated contrast medium is water soluble, it permits excellent tagging homogeneity not only for residual fluid but also for residual stool (6,8,11,21). Ionic iodine-based fecal-tagging CTC studies with minimum laxative cleansing had homogeneity superior to that of nonionic iodine-based fecal-tagging CTC studies without laxative cleansing. Small quantities (10mL) of sodium picosulfate solution were used in the ionic iodine group. However, a nonionic iodine group with minimum laxative cleansing may achieve similar results. As expected, the ionic iodine-based fecal-tagging regimen with minimum laxative resulted in significantly better quality bowel preparation than the two nonlaxative regimens (the barium and nonionic iodine groups). This result might also have been due to the washing effect of the ionic iodine-based contrast agent (11). More stools were found in the barium and nonionic iodine groups than in the ionic iodine group (both P values < .05). More fluid was found in the nonionic iodine group than in the ionic iodine group (P < .05). It was unexpected that there were quality differences in bowel preparation between the two nonlaxative regimens. More stools were found in the barium group than in the nonionic iodine group (P < .05). In contrast, more fluid was found in the nonionic
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iodine group than in the barium group (P < .05). Overall, there were more residual stools or fluid in the nonlaxative regimens than in the minimum-laxative regimen. Dachman et al (34) found that nonlaxative regimens that left significant residual feces, even if well tagged, were not desirable, because greater quantities of feces made the examinations more difficult to interpret. This study was limited in that it was not a prospective study. The bowel preparation (nonlaxative or minimumlaxative, total dose of contrast agents, and duration of preparation) and the scanning protocols were heterogeneous. The use of different CT scanners from different manufactures and slightly different CT parameters, such as the use or not of automatic tube current modulation (35), may have affect the measurements of CT attenuation; however, the CT scanners are regularity calibrated, and thus this effect is predictable and expected to be small. A second limitation is that we did not evaluate the accuracy of colorectal polyp detection, because the limited number of true-positive cases made this impractical. However, our purpose in this study was to evaluate homogeneity for each oral-tagging contrast agent. The results of our study may provide a basis for future assessments of fecal-tagging regimens for CT colonography. Third, we did not evaluate the patients’ acceptance or discomfort regarding the bowel preparation procedure. In conclusion, the iodine-based fecal-tagging regimens provided significantly greater homogeneity in the oral tagging of fecal material than the barium-based fecal-tagging regimen. Iodine-based regimens can provide an appropriate fecal-tagging method for nonlaxative or minimum-laxative CTC studies.
ACKNOWLEDGMENTS
We thank Tomoko Imasawa, MD, Tomoko Obunai, MD, Atsushi Iyama, RT, and Teppei Mikami, RT, for their technical cooperation and Ms Elisabeth Lanzl for assistance in editing this report.
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