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Original Research |
1 Department of Radiology and Research Institute of Radiology, University of
Ulsan College of Medicine, Asan Medical Center, 388-1 Poongnap-Dong,
Songpa-Gu, 138-040 Seoul, Korea.
2 Weill Medical College of Cornell University, New York, NY.
3 Department of Radiology, Seoul National University College of Medicine, Seoul
National University Bundang Hospital, Bundang-gu, Seongnam-si, Korea.
Received March 1, 2007;
accepted after revision October 3, 2007.
Addres correspondence to S. H. Park
(seongho{at}amc.seoul.kr).
Abstract
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MATERIALS AND METHODS.Seventy-four patients were examined with colonos-copy and subsequent CTC (time interval, 0–8 days) using automated CO2 insufflation. Thirty-six patients whose colonoscopy was incomplete due to severe luminal narrowing by cancer that prevented colonoscope passage constituted the stenotic group. The remaining 38 patients constituted the nonstenotic group. Colonic distention was graded by two experienced readers from 1 (worst) to 4 (best) and compared between the two groups. Clinical data and CT images were analyzed for the occurrence of colonic perforation.
RESULTS.Distention was not significantly different between the stenotic and nonstenotic groups in any colonic segments in both supine and prone positions. The mean distention grade ± SD of the colonic segments proximal to the luminal narrowing in the stenotic group (n = 143 segments) was 3.7 ± 0.7 and 3.8 ± 0.7 for the supine and prone positions, respectively. Colonic perforation was not noted in any of the 74 patients, including 65 patients who underwent CTC within 24 hours after colonoscopy (62 snare polypectomies, two polypectomies using biopsy forceps, 63 routine mucosal biopsies).
CONCLUSION.Automated pressure-controlled CO2 insufflation is as efficient in colonic distention for CTC in colorectal cancer patients with severe luminal narrowing as it is in patients without severe luminal narrowing.
Keywords: automated insufflation • colorectal cancer • CT colonography • distention • safety • virtual colonoscopy
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Automated CO2 insufflation operates on a lower infusion pressure than manual insufflation, which has a peak intracolonic pressure ranging from 41 to 148 mm Hg according to an industrial study [7]. In patients with severe luminal narrowing by colon cancer, therefore, there may be potential concerns regarding the effectiveness of automated CO2 insufflation because the severe luminal narrowing may impede low-pressure air flow into the colonic segments proximal to the narrowing. Automated CO2 insufflation has previously been used in scattered patients with occlusive colorectal cancer in large study cohorts [8, 9]. However, to our knowledge, no published studies have specifically investigated the effectiveness of automated CO2 insufflation for colonic distention in patients with occlusive colorectal cancer compared with those who do not have such colonic luminal narrowing.
Colonic perforation during CTC is a rare event. Most of the sporadically reported cases of colonic perforation have been associated with the use of manual insufflation and have generally occurred in symptomatic patients or in those with underlying diseases, including inflammatory bowel disease, colon cancer, and diverticulosis [10–14]. A causal relationship between manual insufflation, as opposed to automated insufflation, and perforation cannot be exactly inferred because it is unknown how many subjects underwent manual versus automated insufflation and because some perforations were attributed to the use of a relatively large and rigid rectal tube, which is different from the small flexible catheter used with automated insufflation, rather than to the manual insufflation itself [9]. The cumulative evidence, however, suggests that the risk of perforation when automated insufflation is used is lower than when manual insufflation is used [9].
CTC is not recommended shortly after colonoscopic polypectomy, particularly after snare polypectomy, or after biopsy because of the increased risk of perforation [10, 15]. Automated pressure-controlled CO2 insufflation with its high safety profile and use of low infusion pressure, however, may possibly be safe even in patients who have recently undergone colonoscopic polypectomy or biopsy.
The purpose of the study, therefore, was to determine the effectiveness of automated CO2 insufflation in colonic distention for CTC in patients with severe luminal narrowing by colorectal cancer and preliminarily evaluate its safety when performed shortly after colonoscopic polypectomy or biopsy.
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Study Population
Between October 2005 and March 2006, 74 consecutive patients (45 men and 29
women; mean age ± SD: men, 56.3 ± 11.2 years; women, 57.2
± 11.6 years) who were referred to our institution for newly diagnosed
colorectal cancer or suspicion of colorectal cancer were referred for optical
colonoscopy (Fig. 1). Optical
colonoscopy was performed by one of five board-certified gastroenterologists,
each with experi ence with more than 1,000 cases. Subsequent CTC was performed
if there was no evidence or suspicion of colonic perforation as judged by the
discrimination of optical colonoscopy–performing gastroenterologists;
patient symptoms and signs, such as abdominal pain, tenderness, or fever; and
laboratory findings, such as leukocytosis, if available. Colonic perforation
was not suspected in any patients; therefore, all 74 patients underwent
subsequent CTC. The time interval between optical colonoscopy and CTC ranged
from 0 to 8 days (median, 0 days).
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CTC
Bowel preparation was performed with 4 L of polyethylene glycol (PEG)
solution (246 mg of PEG) the night before optical colonoscopy. Colonic
inflation during optical colonoscopy was performed with room air. In the 43
patients who underwent optical colonoscopy and CTC on the same day, CTC was
performed 1–4 hours after optical colonoscopy, and the patients were
instructed to evacuate colonic gas and residual fecal matter as much as
possible during the interval between optical colonoscopy and CTC. In the
patients who underwent CTC on different days, 250 mL of magnesium citrate and
10 mg of bisacodyl were also administered the night before CTC, if necessary
(i.e., food intake between optical colonoscopy and CTC). Before CT, a small
catheter with a retention cuff (PROTOCO2L administration set,
E-Z-EM) was placed in the rectum by a dedicated CT technologist. After
inflation of the retention cuff with 20–25 mL of room air, it was gently
pulled back until its proximal end rested on the anal sphincter. Colonic
distention was achieved using CO2 and the automated insufflator
(PROTOCO2L colon insufflator, E-ZEM) under the supervision of a
radiologist. Both the technologist and the radiologist were blinded to whether
the prior optical colonoscopy was complete or incomplete. The maximum rectal
pressure shutdown, beyond which the system automatically stops further
insufflation, was set at 25 mm Hg throughout the procedure.
Insufflation was begun with the patient in the left lateral decubitus position, and the patient then gradually moved to the supine position. A scout view was obtained after suggestive signs of a fully distended colon (i.e., patient's intolerance, initial insufflation of approximately 2–2.5 L, or consistent rectal pressure of more than 25 mm Hg). When distention was suboptimal despite a rectal pressure reading exceeding 25 mm Hg, the extension tube was checked to confirm the absence of any blockage, compression, or kink, and the rectal tube tip was repositioned to avoid possible occlusion of the tip against the rectal wall. If unsuccessful, slight flexion of the patient's knee and hip joints to relax the abdomen, gentle manual palpation of the abdomen, and additional positional changes according to the location of the poorly distended segment or segments were all attempted in each of such patients with additional insufflation.
When an air leak through the anus was suspected, the rectal catheter with retention balloon was tightly pulled back to the anal sphincter by the radiologist throughout the insufflation procedure for a tight closure of the anal opening with the balloon to prevent air leakage. Then the catheter was fastened to the patient's inner thigh immediately before scanning. After completion of the supine scan, insufflation was discontinued and the patient was turned prone. A cushion was placed beneath the patient's lower chest to decrease compression of the abdomen. A prone scout image was obtained. Further insufflation was performed if the distention was deemed suboptimal.
CT scans were obtained using a 16-MDCT scanner (Somatom Sensation 16, Siemens Medical Solutions) with the following parameter settings: beam collimation, 16 x 0.75 mm; slice thickness, 1 mm; reconstruction interval, 0.7 mm; beam pitch, 1; gantry rotation time, 0.5 second; table speed, 24 mm/s; field of view, to fit; 120 kV; and 50–150 mAs, depending on anatomic locations for the supine scan (i.e., the use of automatic dose reduction system [CARE Dose 4D, Siemens Medical Solutions]), and 50 mAs for the prone scan. The supine scan was obtained at a 72-second delay with IV administration of 150 mL of iopromide (Ultravist 370, Bayer HealthCare) at a rate of 2.5 mL/s.
Image Interpretation and Clinical Data
Image analysis was performed using a commercial CTC system (AW version 4.2
with colonography, GE Healthcare) by consensus of two readers (one with
experience of more than 500 cases and the other with experience of
approximately 100 cases) who were blinded to the patient group (i.e., stenotic
vs nonstenotic). The colon was divided into six segments: rectum, sigmoid,
descending, transverse, ascending, and cecum
[16]. The degree of distention
in each segment was assessed in the least distended portion of the segment
using the following 4-point scale used previously by Taylor et al.
[16]: grade 1, complete
collapse; grade 2, partial collapse; grade 3, reasonable but suboptimal
distention; and grade 4, optimal distention (Fig.
2A,
2B,
2C,
2D). Grade 2 was defined as a
situation in which the thickest portion of the haustral folds measured more
than 4 mm in width and met in the lumen, thereby obliterating a clear central
navigation pathway through that segment
[16]. 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 in the
colonic lumen and therefore allowed a clear central navigation path way
[16]. Grade 4 was defined as a
situation in which the colonic wall was pencil-thin throughout the segment
with thin haustral folds less than 2 mm thick throughout their length
[16].
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In colonic segments where a colon cancer mass was present, the longer portion between the proximal and distal portions with respect to the mass was used for grading. For example, when the mass was present in the distal part of the sigmoid colon, the portion of the sigmoid colon proximal to the mass (i.e., the longer portion) was used for grading. After the blinded review, the narrowest diameter of the luminal stenosis by cancer was measured for patients in the stenotic group.
To analyze interobserver agreement in grading the colonic distention, 10 patients from each of the stenotic and nonstenotic groups were randomly selected. Colonic distention in the 20 patients (i.e., 120 colonic segments for each position, supine and prone) was graded by another independent reader (with a case experience of approximately 100) according to the aforementioned method [15].
The number and type of polypectomies, biopsies, or both performed during optical colonoscopy were recorded. In the patients who underwent polypectomy, the size and morphologic type of polypectomized lesions were recorded. A search for extraluminal air was performed at CTC. Patients were observed for abdominal pain, tenderness, and fever after CTC at our inpatient wards until surgery for colorectal cancer or hospital discharge. WBC count was checked if available or if it was to be obtained in cases of suspected colonic perforation. In those who underwent surgery for colorectal cancer, the colon was carefully examined during surgery to determine whether colonic perforation was present.
Statistical Analysis
The frequency of use of the three maneuvers to improve colonic distention
(i.e., flexion of the knee and hip joints, gentle manual palpation of the
abdomen, and additional positional changes) was compared between the stenotic
and nonstenotic groups using the Fisher's exact test. Comparisons with regard
to the degree of colonic distention were made between the stenotic and
nonstenotic groups per colonic segment in the following ways: overall
comparison (e.g., all descending colon in the stenotic group vs all descending
colon in the non stenotic group), comparison of colonic segments of the
stenotic group that were proximal to the severe luminal narrowing versus the
corresponding colonic segments of the nonstenotic group, and comparison of
colonic segments of the stenotic group that were distal to the severe luminal
narrowing versus the corresponding colonic segments of the nonstenotic
group.
The degree of colonic distention was compared between those who underwent CTC and optical colonoscopy on the same day and those who underwent the examinations on different days in the stenotic group. The supine and prone positions were compared separately. Wilcoxon's rank sum test was used for statistical comparisons of colonic distention. Interobserver agreement was evaluated using the weighted kappa statistic and overall proportion of agreement [17]. The kappa statistic was obtained using version 7.3 of MedCalc software (MedCalc), and other statistical analyses were performed with version 11.5 of SPSS software (SPSS). A p value of less than 0.05 was considered to be statistically significant.
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Degree of Colonic Distention
The three maneuvers (i.e., flexion of the knee and hip joints, gentle
manual palpation of the abdomen, and additional positional changes) were
required in three of 34 of the stenotic patients and in eight of 38 of the
nonstenotic patients, showing no statistically significant difference
(p = 0.20). In one of the eight patients in the nonstenotic group,
pulling the retention balloon back to the anal sphincter by the radiologist
during insufflation was also required to prevent air leakage.
The degree of distention in each colonic segment and its overall comparison between the stenotic and nonstenotic groups are summarized in Table 1, showing no statistically significant difference in any colonic segments for both supine and prone positions.
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In the 34 patients of the stenotic group, the narrowest diameter of luminal stenosis resulting from cancer ranged from 1 to 13 mm (mean ± SD, 6.9 ± 3.2 mm). In those patients, 143 colonic segments (sigmoid [n = 23], descending [n = 24], transverse [n = 28], ascending [n = 34], and cecum [n = 34]) were proximal to the luminal narrowing, whereas 61 colonic segments (rectum [n = 34], sigmoid [n = 11], descending [n = 10], and transverse [n = 6]) were distal to the luminal narrowing. The comparison of distention between the colonic segments of the stenotic group and the corresponding colonic segments of the nonstenotic group is summarized in Table 2 (colonic segments proximal to the severe luminal narrowing) and Table 3 (colonic segments distal to the severe luminal narrowing), showing no statistically significant difference in any colonic segments for both supine and prone positions. The total mean colonic distention grade ± SD of the colonic segments proximal to the severe luminal narrowing in the stenotic group (n = 143 segments) was 3.7 ± 0.7 and 3.8 ± 0.7 for the supine and prone positions, respectively. The total mean colonic distention grade ± SD of the colonic segments distal to the severe luminal narrowing in the stenotic group (n = 61 segments) was 3.9 ± 0.4 and 3.8 ± 0.6 for the supine and prone positions, respectively.
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Twenty-two of the 34 patients in the stenotic group underwent CTC on the same day as optical colonoscopy. The mean ± SD of the narrowest diameter of the luminal narrowing was 6.7 ± 3.3 mm for those with same-day optical colonoscopy and CTC (n = 22) and 7.2 ± 3.1 mm for those with different-day optical colonoscopy and CTC (n = 12), showing no statistically significant difference (p = 0.76). The comparison of colonic distention between those with same-day optical colonoscopy and CTC and those with different-day optical colonoscopy and CTC is summarized in Table 4 (colonic segments proximal to the severe luminal narrowing) and Table 5 (colonic segments distal to the severe luminal narrowing). There was no statistically significant difference between the two subgroups in any colonic segments for both supine and prone positions, except for the trans-verse colon that was distal to the luminal narrowing in the prone position (Table 5).
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Interobserver agreement in grading the colonic distention was very high, showing a kappa statistic of 0.775 and 0.816 for supine and prone positions, respectively, and the overall proportion of agreement of 89.2% (107/120) and 90.8% (109/120) for supine and prone positions, respectively. Because most colonic segments of our study patients were basically well distended, the degree of colonic distention of the 20 patients showed a markedly skewed distribution, with most of the colonic segments being graded 4 by all readers: 95 of 120 and 98 of 120 segments in supine and prone positions, respectively, were graded 4 by all readers.
Summary of Colonoscopic Polypectomy and Biopsy and Follow-Up After CTC
A total of 76 snare polypectomies, two polypectomies using biopsy forceps,
and 73 routine mucosal biopsies using biopsy forceps were performed in the 74
patients: both routine mucosal biopsy and polypectomy (1–11 polyps) in
20 patients, polypectomy only in two patients (one and 11 polyps,
respectively), and routine mucosal biopsy only in 52 patients. The time
interval between optical colonoscopy and CTC was 0 (i.e., on the same day) to
3 days in the 20 patients who underwent both routine mucosal biopsy and poly
pectomy, 0 days in the two patients who underwent polypectomy only, and
0–8 days in the 52 patients who underwent routine mucosal biopsy only.
Sixty-five of the 74 patients underwent CTC within 24 hours after optical
colonoscopy with a total of 62 snare polypectomies, two polypectomies using
biopsy forceps, and 63 routine mucosal biopsies. Both routine mucosal biopsy
and polypectomy (1–8 polyps) were performed in 17 patients, polypectomy
only in two patients (one and 11 polyps, respectively), and routine mucosal
biopsy only in 46 patients.
The 78 lesions that were removed with polypectomy were measured (mean ± SD) at optical colonoscopy to be 6.0 ± 3.7 mm (range, 1–20 mm) and consisted of 64 sessile and 14 pedunculated polyps. The 64 polypectomized lesions in those patients who underwent CTC within 24 hours after optical colonoscopy were measured at optical colonoscopy to be 5.4 ± 2.6 mm (range, 1–15 mm) and consisted of 51 sessile and 13 pedunculated polyps.
Extraluminal gas was not noted at CTC in any patients. No patient developed abdominal pain, tenderness, or fever after CTC until surgery for colon cancer (n = 64, 1–10 days) or hospital discharge (n = 10, 2–12 days). WBC count, obtained 0–13 days (mean ± SD, 2.9 ± 2.5 days) after CTC, was available in 61 patients and was normal in all patients. The 64 patients who underwent surgery showed no evidence of colonic perforation at surgery.
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In our study, we evaluated the effectiveness of automated CO2 insufflation in colonic distention for CTC in colorectal cancer patients with severe colonic luminal narrowing using a 4-point grading system [16]. The interobserver agreement of the grading system for colonic distention was shown to be excellent considering the prevalence effect [22, 23] on the kappa statistic by the skewed distribution of the degree of colonic distention in our test data set (i.e., kappa is small despite a high agreement if the population distribution is skewed). Our results clearly show that automated CO2 insufflation is an effective method of colonic distention for CTC, even in patients with severe luminal narrowing. The degree of colonic distention of both the proximal and distal colonic segments with respect to the severe luminal narrowing in the stenotic group was not significantly different from the distention of the corresponding colonic segments in the nonstenotic group.
The frequency of patients who required the three maneuvers to help improve colonic distention was also not significantly different between the stenotic and nonstenotic groups. Moreover, the mean distention grade ± SD of the colonic segments proximal to the severe luminal narrowing was 3.7 ± 0.7 and 3.8 ± 0.7 for the supine and prone positions, respectively, representing almost optimal distention. The mean distention grades were comparable with—in fact, even higher than—those of a previous study [4] where automated CO2 insufflation resulted in 3.20 ± 1.16 and 3.22 ± 1.12 grades of colonic distention for the supine and prone positions, respectively.
Although automated CO2 insufflation is generally effective for colonic distention in both stenotic and nonstenotic patients, maneuvers such as flexion of the knee and hip joints, gentle manual palpation of the abdomen, and additional positional changes may be of help in patients with difficult distention, as shown by 11 patients in our study. The interpretation of the association between the maneuvers and improved colonic distention, however, is somewhat limited because our study was not optimally designed to evaluate the effect of each maneuver on colonic distention. Because our main study purpose was to determine the effectiveness of automated CO2 insufflation in patients with occlusive cancer when it was used at its full capacity (i.e., when used in combination with all other practical means to improve colonic distention if necessary), we used all three maneuvers in each patient with difficult distention. Therefore, the effect of each specific maneuver could not be evaluated separately. We also did not use pro cedures suggested by others as a means to improve colonic distention such as initial 360° turning during insufflation [24] or placement of an additional pillow under the pelvis and thighs [15]. Whether such procedures might have made our maneuvers unnecessary is not certain. Evaluation of the effect of each of our maneuvers in assisting colonic distention may be worth further studies.
We did not acquire a baseline CT image or scout CT image before the initiation of CO2 insufflation, which would have enabled us to assess the amount of residual colonic air that had been infused during optical colonoscopy, to minimize patient radiation exposure. A systematic analysis of the amount of residual colonic air and its effect on the degree of colonic distention, therefore, was not possible. However, the effect of the remaining colonic air after optical colonoscopy on colonic distention was most likely insignificant because patients were instructed to evacuate colonic gas and residual fecal matter as much as possible during the interval between optical colonoscopy and CTC. In fact, our results that colonic distention (and the luminal diameter of the point of narrowing) between those who underwent CTC and optical colonoscopy on the same day and those who underwent the examinations on different days in the stenotic group was not significantly different in virtually all colonic segments (except for the transverse colon that was distal to the luminal stenosis in the prone position) show that the effect of the remaining colonic air was insignificant.
Performance of CTC shortly after colonoscopic polypectomy or biopsy is not recommended because of the risk of colonic perfo-ration [10, 15]. Investigators have performed studies regarding the healing time after colonic wall injury and the safety interval between invasive colonoscopic procedure and barium enema [25–28]. However, similar information that is specific to CTC, especially with the use of automated CO2 insufflation, to our knowledge, is not available. Several studies [25, 26] have suggested that barium enema should be delayed at least 6 days after a deep biopsy (i.e., injury farther than the submucosa) or polypectomy using electrocautery, although it may be performed without delay after superficial biopsy in most cases. Researchers have also suggested that a time delay of longer than 1 week may be required until the follow-up colonic examination because 1 week represents the time of maximal granulation tissue formation in most surgical wounds and the injured colonic wall is paradoxically weakest at that time [15]. Another study [27] of 833 patients who underwent colonoscopic polypectomy or biopsy and subsequent barium enema, including 722 barium enema studies performed within 72 hours of the colonoscopic polypectomy or biopsy (same day, n = 5; within 24 hours, n = 543; and within 72 hours, n = 174), however, suggested no need for time restriction between the examinations.
Considering that there is inherent safeguard for pressure control in the automated CO2 insufflation system [9] and that perforation associated with CTC may not be as devastating as that associated with barium enema (i.e., barium peritonitis) [29], pressure-monitored automated CO2 insufflation is expected to be performed relatively more safely than barium enema after colonoscopic polypectomy or biopsy, as preliminarily shown in our small number of patients. However, given that the occurrence of colonic perforation during CTC is an extremely rare event with a symptomatic perforation incidence ranging from 0.005% to 0.05% [8–10], our results from a small population are by no means sufficient to make any conclusion regarding the safety of CTC using automated CO2 insufflation performed shortly after polypectomy or biopsy.
Same-day performance of optical colonos-copy and CTC is an apparent convenience to patients; however, in patients who have undergone polypectomy or biopsy, it has several other problems in addition to the safety issue. Colonic perforation can occur after optical colonoscopy, particularly when performed with polypectomy or biopsy, and may go undetected. Then, its discovery after follow-up CTC may lead to the false attribution of perfo-ration to CTC. More importantly, CTC may worsen the colonic perforation. Strict confirmation of the absence of colonic perforation before CTC is, therefore, necessary and would require additional baseline abdominal CT and concomitant radiation exposure because a scout image is generally unlikely to be sensitive enough to depict a small amount of extraluminal gas [15, 30, 31]. Therefore, it is not certain whether same-day optical colonoscopy and CTC are appropriate in patients who have undergone polypectomy or biopsy even if the safety should be supported by further data.
Our study has limitations. First, although we did not acquire a baseline CT image or scout image to minimize radiation exposure to the patient, an improved study design should include baseline CT. This additional image is required to exclude the patients who were already perforated during optical colon-o scopy and to clearly prove which examination is responsible if perforation is found after CTC. As we mentioned previously, a baseline scout image is probably not useful because it is generally not sensitive enough to depict small amounts of extraluminal gas [15, 30, 31].
Second, we evaluated the end result of the insufflation procedure (i.e., degree of colonic distention) to prove the effectiveness of automated CO2 insufflation in colonic distention for CTC in patients with severe luminal narrowing by cancer. Evaluation of the effectiveness of the entire insufflation procedure, however, may also include comparison of other factors, such as the amount of CO2 and time required to achieve optimal distention and the level of distention-associated patient discomfort between those with and those without severe luminal stenosis. Such information would have made our study results more scientific and more useful for clinical practice. Although patient discomfort was not evaluated precisely in our study, none of the patients complained of severe discomfort to the degree at which continuation of the examination was not possible.
Third, although 25 mm Hg of maximum rectal pressure shutdown was consistently used throughout the study, the actual maximum rectal pressure that was achieved (at least temporarily) during CTC was not recorded. Although rectal pressure is an imperfect indicator of the varying intraluminal pressure of each colonic segment, the measurement of the maximum rectal pressure may have provided more precise information regarding the acceptable degree of intraluminal pressure.
Finally, although the readers were blinded with regard to the presence of severe luminal narrowing that had blocked colonoscope passage, a completely blinded study was not technically feasible because the CT findings themselves (i.e., degree of luminal narrowing at CT) may suggest the possibility of such an occurrence. The readers, however, graded the distention in an unbiased way by strict adherence to a previously published method [15].
In conclusion, automated pressure-controlled CO2 insufflation is as efficient in colonic distention for CTC in colorectal cancer patients with severe luminal narrowing as it is in patients without severe luminal narrowing.
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