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Original Research |
1 Department of Intestinal Imaging, St. Mark's and Northwick Park Hospitals,
Harrow, United Kingdom HA1 3UJ.
2 Present address: Department of Imaging, University College Hospital, 235
Euston Rd., London, United Kingdom NW1 2BU.
Received September 24, 2004;
accepted after revision January 11, 2005.
Address correspondence to S. A. Taylor.
Abstract
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SUBJECTS AND METHODS. One hundred forty-one symptomatic subjects underwent CT colonography using either an automated device (n = 47) or a manual method (n = 94) for carbon dioxide insufflation. CT data sets were assessed retrospectively in consensus by two blinded observers who graded distention for six colonic segments using a 4-point scale. An additional assessment of the overall clinical adequacy of distention (yes/no) was also made, and any learning curve was sought. Each patient completed a validated 24-point patient questionnaire reflecting patient satisfaction and discomfort. Distention scores, clinical adequacy, and questionnaire responses were analyzed using ordered logistic regression, Fisher's exact test, and the Mann-Whitney test statistic, respectively.
RESULTS. Automated insufflation significantly improved distention overall (p = 0.001). For individual segments, distention was significantly improved in the sigmoid (p = 0.007) and descending (p < 0.001) colons when the patient was supine; and in the sigmoid (p = 0.02), descending (p = 0.001), and transverse (p = 0.02) colons when supine and prone positions were combined. No significant difference was seen in the clinical adequacy of distention, nor was there evidence of any learning curve for either insufflation method. Subjects were more weary after automated insufflation (p = 0.03), but no significant difference was seen for the remaining 23 questionnaire items or for feelings of bloating or discomfort.
CONCLUSION. Automated carbon dioxide insufflation significantly improves colonic distention compared with manual insufflation. Benefit is greatest in the left colon, particularly when the patient is supine. Patient acceptance is similar to that for manual insufflation.
Keywords: carbon dioxide • colon • colonography • CT • MDCT colonography
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Use of an automated carbon dioxide insufflation device to facilitate optimal distention has been proposed (Yee J et al., presented at the 2002 meeting of the Radiological Society of North America [RSNA]). Data from the barium enema and endoscopy literature show that carbon dioxide causes less abdominal cramping than air [8, 9] and is therefore already widely used for CT colonography [2, 10–12]. Advocates of automated insufflation suggest that introducing carbon dioxide at controlled flow rates and pressures improves patient compliance and overall distention, producing robust, reproducible results in the absence of significant prior user experience. To date, however, the device has been compared only with manual insufflation of room air (Yee et al., presented at the 2002 RSNA meeting), and consequently it is unclear whether the benefit of automated insufflation is merely a result of using carbon dioxide. At the time of this writing, no published data have evaluated the effectiveness and acceptance of automated insufflation versus manual insufflation when carbon dioxide is used for both. The purpose of our study was to compare the effects of automated and manual carbon dioxide insufflation on luminal distention before MDCT colonography, to investigate any user learning curve, and to assess the patient acceptance of both methods.
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Additional historical controls were then selected from a database of 168 symptomatic patients who had undergone manual carbon dioxide insufflation before CT colonography in a previous comparative trial with colonoscopy conducted between January 2001 and December 2002. All patients were undergoing investigation for suspected colorectal neoplasia and were recruited from the same outpatient source as for the comparative trial with barium enema (which provides the study group as described above). Only patients who had received a spasmolytic and were older than 60 years were eligible as controls, in an attempt to match the study group as far as possible. After database review, 66 patients were added to the initial 28 patients described previously, so that the control group comprised 94 patients (49 women, 45 men; mean age, 69.6 years [± 7.8 years]; age range, 60–85 years). Both trials had full ethical approval from our institutional review board, and patients gave explicit written consent for this comparative study.
Bowel Preparation
All patients were instructed to maintain a clear liquid diet 24 hr before
their appointment and underwent full bowel preparation with either two packets
of magnesium citrate (Citramag, Pharmaserve) supplemented with one packet of
senna granules (Senokot, Reckitt Benckiser Healthcare) (36 control subjects)
or two packets of sodium picosulfate (Picolax, Ferring Pharmaceuticals) (all
47 of the study group and 58 control subjects).
CT Colonography
Patients were asked to lie on the CT scanner table, and 20 mg of hyoscine
butylbromide (Buscopan, Boehringer Ingelheim) was administered IV unless
contraindicated (recent symptomatic ischemic heart disease or history of
closed-angle glaucoma), in which case glucagon hydrochloride (GlucaGen
HypoKit, Novo Nordisk Pharmaceuticals) was administered. In total, two of 47
in the study group received glucagon hydrochloride, and all control subjects
received hyoscine butylbromide. Patients then turned into the left lateral
position facing away from the operator, and a lubricated catheter was inserted
into the rectum and taped to the patient's buttocks. Colonic insufflation of
carbon dioxide was then performed either using the automated device (study
group) or manually (control group), as discussed in the following text.
After insufflation, a CT scout scan was obtained before both supine and prone data acquisitions to assess distention adequacy and to provide an opportunity for further gas administration if necessary. CT was then performed using a 4-MDCT scanner (LightSpeed Plus, GE Healthcare) with the following parameters: 1.25- to 2.5-mm collimation; pitch, 1.5; 120 kVp; 50–100 mA; and 50% slice overlap. Images were reconstructed at half the nominal slice thickness.
Colorectal Insufflation: Study Group
Automated insufflation was supervised by a single operator (a radiology
resident) with no previous experience with CT colonography and was achieved
using the Protocol insufflation system (E-Z-EM). An inexperienced operator was
deliberately chosen in order to mimic the real-life implementation of an
insufflation device in CT colonographic practice and to permit assessment of
any learning curve associated with the technique. The operator had undergone a
1-hr hands-on tutorial with the equipment manufacturer before using the
device. The insufflation system electronically controls the flow rate of
carbon dioxide between 1 and 3 L/min and displays the total volume of gas
administered (updated continuously). If intracolonic pressure (measured at the
rectal catheter tip) increases beyond the limit set by the user, up to a
maximum of 25 mm Hg, the system automatically shuts down to prevent further
insufflation.
In general, the pressure dial was set at 25 mm Hg, or less if the patient complained of significant abdominal discomfort. Insufflation was begun with the patient in the left lateral position; after approximately 1.5 L, the patient was turned either prone (the first 23 study patients) or supine (the last 24 study patients). Colonic distention was continued according to patient tolerance and was sustained if rectal pressure remained low (< 15 mm Hg), providing the patient did not complain of undue abdominal discomfort. Gas insufflation was then paused, by pressing a button, before the first CT scout image was obtained. If the scout image suggested areas of collapse, insufflation was recommenced, again according to patient tolerance and intracolonic pressure. For the second scanning position, another scout image was obtained, again with the opportunity for further insufflation if distention was deemed suboptimal. For each individual, the volume of carbon dioxide delivered was recorded immediately before formal prone and supine scanning acquisitions.
Colorectal Insufflation: Control Group
Manual insufflation was performed by a different single operator (a
radiology resident) and was achieved using a standard enema bag filled with
approximately 3 L of carbon dioxide. The operator initially had no prior
experience of CT colonography but was experienced in the bag insufflation
system from previous barium enema work. The filled bag was attached to a
rectal catheter via a connecting tube that could be sealed with a plastic
clip. Insufflation was achieved via gentle manual compression of the enema bag
over 2–3 min, commencing with the patient in the left lateral position.
When the bag was approximately half empty, the patient was turned prone and
insufflation was continued to maximal patient tolerance or until the enema bag
was empty. As with the automated device, further gas was insufflated before
both the prone and supine scanning acquisitions, depending on the CT scout
images. The operator was free to resort to administration of room air,
introduced via an insufflation bulb attached to the rectal tube, if the scout
image suggested suboptimal distention and the enema bag was empty of carbon
dioxide.
For both insufflation methods, rectal catheters remained in situ until both prone and supine scans had been obtained.
Image Analysis
Image analysis was performed using a dedicated workstation with proprietary
software (Advantage Windows 4.0 and Colonography, GE Healthcare). The axial
prone and supine 2D data sets were displayed side by side in the upper half of
the workstation screen while multiplanar reformations were simultaneously
displayed in the lower half. Two nonobservers loaded data sets from the study
and control groups onto the workstation in random order. Two observers then
retrospectively analyzed the data sets in consensus, fully blinded to the
insufflation method used and unaware that two insufflation systems were being
compared. The observers were competent in abdominal CT but had little prior
experience of CT colonography. Each underwent a 4-hr training period from a
radiologist who was experienced in CT colonography and who demonstrated the
technique of colon tracking on 2D scrolling and explained the distention
grading system in detail.
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Distention for each of these six segments was assessed by examining the 2D displays and was graded using a 4-point scale modified from a system used by Taylor et al. [5] that was itself initially based on work by Chen et al. [4] (Figs. 1A, 1B, 1C, and 1D): grade 1 indicated complete collapse; grade 2, partial collapse; grade 3, reasonable but suboptimal distention; and grade 4, optimal distention. Partial collapse (grade 2) was defined as a situation in which the thickest portion of the haustral folds (plicae semilunares) measured more than 4 mm in width and met within the lumen, thereby obliterating a clear central navigation pathway through that segment. Reasonable but suboptimal distention (grade 3) was defined as an easily visible colon wall with slightly thickened haustral folds that measured, on average, 2 mm in their widest portion but did not meet and obliterate a central pathway through the segment. Optimal distention was defined as when the colonic wall was thin and sharp, with haustral folds measuring less than 2 mm thick, throughout the segment. A simple categoric yes or no judgment was also made for whether each segment was deemed clinically adequately distended (when supine and prone data sets were combined side by side). Adequate distention was defined as when the observer believed it was possible to confidently exclude polyps larger than 5 mm. The observers were told to ignore the detrimental effects of residual fluid and feces on segmental visualization and to concentrate solely on the adequacy of distention. In view of the relative inexperience of the observers in CT colonography, they were instructed to make this assessment by deciding whether, when combining supine and prone data sets, the whole segment was adequately distended so that a sphere of at least 6 mm added to the colonic lumen would theoretically be visible at all points in the segment.
To assess the reliability and reproducibility of the distention scores from the two observers, a second independent assessment of 50 subjects (600 individual segments), selected using a computer-generated random number table, was made by an additional blinded radiologist who was experienced in more than 400 endoscopically validated CT colonography examinations. This experienced observer was unaware of the consensus distention scores assigned by the two study observers.
Patient Acceptance
A previously validated questionnaire derived from responses to detailed
interviews from patients undergoing full colonoscopy was administered to both
control and study groups to determine the subjective experience of CT
colonography [13]. The
original questionnaire consisted of 25 individual items presented with its
opposite, which were separated by a 7-point scale. One item (pertaining to
sedation) was removed from the original 25-point questionnaire because it was
not relevant to CT colonography. The remaining 24 individual items can be
grouped into three main components, identified using the technique of
principal component analysis: satisfaction, worry, and physical discomfort.
Patients were instructed to place a cross in one of seven boxes lying between
each item and its opposite, depending on their rating for the particular item
(with a higher score indicating a more positive response). The questionnaire
also included a 10-cm visual analogue scale drawn between "no
bloating" and "severe bloating" and between "no
discomfort" and "severe discomfort." Patients were asked to
place a mark on the analogue scale for each item that reflected their
experience, with responses requested for both during and after the procedure.
Questionnaires were administered to patients within 30 min of the scanning
completion, with instructions to return completed questionnaires to the
radiology reception staff.
Statistical Analysis
All statistical analysis was performed using Stata software (version 7,
StataCorp). Distention scores were regarded as a categoric variable and were
analyzed using ordered logistic regression. The scores for both insufflation
methods were compared for each segment in each scanning position and then for
each segment combining the supine and prone positions. An overall comparison
was then made combining all segments and both scanning positions.
Robust SEs were used to account for the relative lack of independence between segmental distention in the same individual. Differences between the two groups were summarized by odds ratios—that is, the odds of being in the next highest (better) distention grade for the study group relative to controls, together with the corresponding 95% confidence interval (CI). The overall clinical adequacy of distention for each segment (recorded as a yes or no response by the observers) was analyzed using Fisher's exact test.
To assess any potential learning curve for both operators, the distention scores and the overall adequacy of distention judgments were reanalyzed after dividing both the study and control groups into two halves chronologically and comparing the first data sets with the second. The effect of distending the colon in either the supine or the prone position first was analyzed by adding this variable to the basic regression model. The effect of total volume on distention scores for the study group was also analyzed using ordered logistic regression with robust SEs used when both scans were combined. The differences in total volume between scans that were and were not deemed to be adequate were assessed using Student's t tests. Questionnaire responses were collated and compared using the Mann-Whitney test.
Statistical significance was assigned at the level of p less than
0.05. Interobserver agreement between distention scores was assessed using the
weighted kappa statistic, defined as poor (< 0.2), fair (> 0.2 to 
0.4), moderate (> 0.4 to 0.6), good (> 0.6 to 0.8), and very
good (> 0.8 to 1) agreement.
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Reproducibility
Comparison of distention scores between the two observers and the
experienced radiologists gave a weighted kappa value of 0.65 (95% CI,
0.59–0.72), indicating good agreement.
Distention
The mean distention scores for the study group (automated insufflation)
were 3.20 (SD, 1.16) and 3.22 (1.12) for the supine and prone scanning
positions, respectively, versus 2.86 (1.27) and 3.00 (1.20) for the control
group (manual insufflation).
Table 1 summarizes the comparison for individual segments in each scanning position and for both scanning positions combined. For supine scanning, automated insufflation resulted in significantly better distention than the manual method for both the sigmoid (p = 0.007) and descending (p < 0.001) colons. The odds of being in the next highest distention category were more than 2.5 times higher for the sigmoid, and more than 4 times higher for the descending colon, using automated insufflation. No significant differences in distention were seen between insufflation methods for the remaining four colon segments for either the supine or the prone position.
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For prone and supine scans combined, distention was significantly better using the automated insufflator for the sigmoid (p = 0.02), descending (p < 0.001), and transverse (p = 0.02) colons. No significant difference was seen for the remaining three segments.
When overall distention scores were considered (combining all segments and both scanning positions), distention was significantly greater using the automated insufflator than the manual method (odds ratio, 1.81 [95% CI, 1.29–2.54]) (p < 0.001).
Adequacy of Scan
Table 2 summarizes the
number and percentage of patients, in both study and control populations, in
whom the distention was judged clinically adequate for individual colon
segments. The results indicate that, overall, a high proportion of segments
were judged to be clinically adequately distended and that no significant
differences were seen between the two insufflation methods.
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Learning Curves
The results for both the study and control groups indicated that no
significant difference existed in either distention score or scan adequacy
between the first and second halves of examinations when placed in chronologic
order, suggesting there was no trend toward improved distention with increased
experience. This was also the case when the supine and prone scans were
examined separately (control group, supine and prone, p =
0.23–0.85 and p = 0.39–0.87, respectively; study group,
supine and prone, p = 0.11–0.88 and p =
0.35–0.86, respectively), and when the two scans were combined (control
group, p = 0.21–0.88; study group, p =
0.31–0.87).
Patient Positioning
For the study population, no significant difference was seen in either
distention score or scan adequacy between examinations whether the patient was
initially scanned prone or supine. This was also the case when the supine and
prone scans were examined separately (supine and prone, p =
0.3–1.0, and p = 0.43–0.95, respectively) and when the
two scans were combined (p = 0.43–0.92).
Volume of Carbon Dioxide Administered Using Automated Insufflation
Carbon dioxide volumes administered before the first scanning acquisition
ranged between 1.9 and 4.5 L (median, 3 L); the total volume administered
(recorded before the second scanning acquisition) ranged between 2.6 and 8.0 L
(median, 4.2 L).
The relationships between total carbon dioxide volumes administered and luminal distention scores are summarized in Table 3. For the supine scanning position, no statistically significant association occurred between larger volumes and distention grade. However, for the prone scanning, larger volumes were associated with significantly poorer distention grades for the sigmoid colon, descending colon, and cecum. For these colon segments, the odds of being in the next highest distention grade were approximately halved by each 1-L increase in total volume. For prone and supine scans combined, increasing volume was associated with significantly poorer distention in the sigmoid colon and cecum. When assessing the effect of total volume on judgments of clinically adequate distention, we found that the mean volume of carbon dioxide administered was significantly higher for inadequately distended segments than for adequately distended segments for the sigmoid (p = 0.02) and ascending (p = 0.008) colon segments, but that there were no significant differences for the remaining segments.
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Patient Acceptance
In total, all 47 study patients and 86 (91%) of 94 control patients
completed the questionnaire. Table
4 summarizes the responses to the individual items by patients in
both study and control groups. Patients' experiences were generally positive.
The only significant difference between the study and control groups was that
patients were more weary after automated insufflation (p = 0.03). The
responses to the remaining 23 of the 24 items were not significantly
different, nor were the responses to the visual analogue scale.
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We found significantly better luminal distention overall using automated administration than using the manual method. The effect was particularly marked for the left colon when the patient was in the supine position and for the transverse colon when both supine and prone scans were combined. This finding supports previous data (Yee et al., presented at the 2002 RSNA meeting) that showed significantly better distention when using the insufflator for all colon segments in the supine position; these data compared automated administration of carbon dioxide with manual insufflation of room air. Interestingly, like Yee et al. [1], we found no significant improvement in distention for any colon segment in the prone position.
Previous work has shown that distention is generally better in the prone than in the supine position [1, 4, 7], and it may be that this positional advantage is sufficiently large to outweigh any smaller benefit of automated insufflation when prone. The reasons for improved distention using automated insufflation may be related to the more controlled method of carbon dioxide delivery, allowing greater volumes to be introduced before maximum patient tolerance is reached. Certainly, that the insufflator stops with higher colonic pressures (e.g., because of segmental spasm) is an advantage over manual insufflation, which does not take account of colonic pressure.
Perhaps more important is the ability of the device to maintain a constant pressure in the colon via intermittent gas insufflation, even during scanning if necessary, which may also in part overcome the potential problem of carbon dioxide reabsorption after manual insufflation.
One could argue that the importance of the improved distention achieved with automated insufflation is questionable because no significant difference was seen between automated and manual insufflation methods for clinical adequacy when supine and prone scans were viewed in combination. However, the observers were deliberately told to ignore fluid and fecal residue in the colon (to avoid bowel preparation as a cofounder). A segment would still be classified as adequately distended if a section was collapsed in one scan orientation but well distended, although partially fluid-filled, in the other. In the clinical environment, however, this segment would not have been fully visualized because of the residual fluid covering a proportion of the mucosa. Clearly, in the absence of perfect colonic preparation, distention should ideally be optimal in both scanning orientations.
Furthermore, optimal distention improves reviewer confidence—for example, by facilitating assessment of movement of a possible polyp between scanning orientations—and thereby decreases reporting times. Whether the benefit in distention justifies the cost of the automated insufflator is beyond the scope of the present study. Such a cost–benefit analysis would be relatively complex and would involve comparing manual and automated insufflation in terms of costs associated with the personnel required, recall rates due to poor distention, costs of endoscopy due to CT colonography false-positives as a result of poor distention, and so forth. Furthermore, the presumed general benefits of carbon dioxide over air in terms of general patient compliance would have to be considered in any analysis.
We found no clear evidence supporting the initial use of one scanning position over the other to improve overall distention.
The volume of gas required to achieve optimal colonic distention varies
according to colon anatomy, patient tolerance and continence, and small-bowel
reflux. In our study, the median volume of carbon dioxide administered for
patients undergoing automated insufflation was 4.2 L. This volume is
approximately twice the 2 L recommended by other authors
[2] and greater than the
manufacturer's technical recommendation (
3 L), albeit smaller than in the
abstracted literature (mean, 6.3 L [Yee et al., 2002 RSNA meeting]). It may at
first appear counterintuitive that we found larger insufflator-administered
volumes were associated with worse distention. However, such large volumes
almost certainly reflect either anal leakage or small-bowel reflux because of
an incompetent ileocecal valve, both of which would serve to reduce
distention. Given that the maximum volume of carbon dioxide contained in an
enema bag is limited to approximately 3 L, the difference in distention
between the two insufflation methods may in part be explained by insufficient
gas available for the manual method. However, the manual operator needed to
administer additional room air in only a single patient in our study.
Good evidence exists that, in general, patients prefer CT colonography to both colonoscopy and barium enema [12, 15, 16]. It would be problematic if automated insufflation improved distention at the expense of patient tolerance. Using a validated questionnaire, we found that patient acceptance was similar for both insufflation methods, and, in particular, no significant differences were seen for either bloating or discomfort. Patients were significantly more weary after automated insufflation (p = 0.03). The reason for this is not clear and, because it was the only difference between the two methods, may likely be explained by a type 1 statistical error because a total of 28 individual comparisons were made. The generally good patient acceptance of both techniques may have been in part due to our use of a spasmolytic. However, interestingly, previous work has not shown any particular effect of hyoscine butylbromide on patient experience with CT colonography [12]. It therefore seems that the use of carbon dioxide rather than air may have contributed to the generally good patient tolerance of both the manual and automated techniques.
The operator using the automated insufflator did not report any undue technical difficulties, although previous workers have described problems maintaining steady flow of carbon dioxide in patients with tortuous or fluid-filled colons [16]. However, those comparisons used a laparoscopic insufflator device that was not tailored to colonic insufflation, and no distention data were accrued. Reassuringly, we found no evidence of a learning curve for either method, suggesting that reasonable results can be expected immediately on introduction.
Our study does have potential weaknesses. All patients but two received IV hyoscine butylbromide to avoid any confounding effect of spasmolytic on distention scores. Therefore, the study does show an advantage of the insufflator, even in patients in whom distention has been optimized in all other ways. Although it is tempting to extrapolate this advantage to patients who were not given hyoscine butyl bromide, we acknowledge that to do so is not fully justifiable, and clearly further studies are required to assess the performance of the insufflator in patients not given a spasmolytic. As a result, this study may be slightly less relevant in the United States, where hyoscine butyl bromide is not licensed.
Patient recruitment was not randomized and most of our controls were historical. However, all patients and controls were 60 years old or older, were undergoing investigation for symptoms of colorectal neoplasia, and were recruited from the same outpatient source. Although no statistically significant difference was seen in patient age or sex between controls and the intervention group, we cannot completely exclude subtle differences.
Not all patients received the same bowel preparation, which may also potentially weaken our conclusions. However, previous work has shown no influence on colonic distention from the two regimens used in our study, so it seems unlikely this was a major confounder [5].
We used different operators to administer gas in each group. However, both operators were initially equally inexperienced in CT colonography, although the operator performing manual insufflation had prior experience of this technique when performing barium enemas. Therefore, any initial benefit in distention due to operator experience might be expected to favor the control population. Moreover, no evidence was seen of a learning curve for either insufflation method, so we think our choice of relatively inexperienced operators did not adversely affect the results. Furthermore, our data suggest that good distention is achievable without significant prior experience.
Our assessment of learning curves could have been confounded by the change in initial scanning orientation approximately halfway through recruitment. However, we found no effect on either segmental or overall distention scores when this variable was examined. Anecdotally, we found manual carbon dioxide insufflation relatively complicated and time-consuming when compared with the automated device, but we did not quantify this in any way.
Finally, we used two observers who were relatively inexperienced in CT colonography to grade the distention, which may theoretically have affected the results. This was done to ensure the observers were absolutely blinded to the scan data and study aims, which would have been unlikely if our more experienced radiologists were used, all of whom had been involved in interpreting data sets from the source trials for the present study. We did not require the observers to interpret the scans for pathology, and both were otherwise experienced CT radiologists, fully trained in the grading system used, which itself has been validated to be robust among observers of differing experience [5]. Furthermore, at the end of the training period, the experienced CT colonographer was reassured that the observers were correctly grading distention. We also showed good agreement in distention scores between the observers and a CT colonography expert for a random set of 50 data sets, providing good statistical evidence that our observers were reliable.
In conclusion, using an automated carbon dioxide insufflation device is associated with significantly improved colonic distention compared with manual insufflation, without detrimental effects for 27 of the 28 patient acceptance questionnaire items. Benefit is greatest in the left colon with the patient supine. No evidence was seen of a significant learning curve with the device.
Acknowledgments
We thank E-Z-EM, Inc. (Westbury, NY) and GE Healthcare (Milwaukee, WI) for
providing the electronic insufflator and CT colonography interpretation
software for this study.
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