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Original Research |
1 Department of Radiology, University of Wisconsin Medical School, E3/311
Clinical Science Center, 600 Highland Ave., Madison, WI 53792-3252.
2 Department of Radiology, Uniformed Services University of the Health Sciences,
Bethesda, MD.
Received July 9, 2007;
accepted after revision September 10, 2007.
P. J. Pickhardt is a consultant for Viatronix, Medicsight, and Fleet.
Abstract
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MATERIALS AND METHODS. The study population consisted of 5,368 adults (mean age, 57.4 years; 2,807 women, 2,561 men) undergoing CTC. Pertinent medical history, CTC imaging studies, and clinic course were reviewed for all cases in which pneumatosis (i.e., air in the bowel wall) was prospectively identified.
RESULTS. Colonic pneumatosis was seen in six (0.11%) of 5,368 total CTC studies. No cases of small-bowel pneumatosis were identified. There were no cases of frank colonic perforation in this series. All six cases of pneumatosis involved the use of automated carbon dioxide for colonic distention (0.17%; six of 3,451 cases). Pneumatosis was not seen in 1,917 cases with manual room air insufflation (p = 0.095). The right colon was involved in all cases, typically revealing a thin curvilinear configuration with variable circumferential extension. In one of the six cases, a frankly cystic appearance (pneumatosis cystoides intestinalis) was seen in the left colon. No free intraperitoneal gas, portomesenteric venous gas, or distant extraperitoneal gas was present in any case. No unexpected abdominal symptoms developed during the CTC examination, and all six patients were asymptomatic after the procedure. None of the patients required any treatment or intervention.
CONCLUSION. Asymptomatic right-sided colonic pneumatosis is a rare self-limited condition associated with carbon dioxide delivery at CTC. This benign imaging finding should not be confused with symptomatic perforation.
Keywords: complications • CT colonography • perforation • pneumatosis • virtual colonoscopy
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Study Population
A total of 5,368 adults (2,807 women and 2,561 men; mean age, 57.4 years)
undergoing CTC examination composed the main study group. The indication for
CTC was primary screening evaluation in 5,125 patients and diagnostic for
previous incomplete optical colonoscopy in 243. No patients undergoing CTC
were excluded from this evaluation.
Colonic Preparation
Bowel preparation before CTC entailed a clearliquid diet the day before
examination, including the oral administration of sodium phosphate, 2% barium
suspension, and diatrizoate. Magnesium citrate was substituted for sodium
phosphate in patients with known or suspected renal or cardiac insufficiency.
In rare cases, polyethylene glycol was used as the cathartic agent in patients
unable to tolerate any fluid shifts.
Colonic Distention
Colonic distention was achieved via a small flexible rectal catheter by
either manual insufflation of room air (n = 1,917) or automated
carbon dioxide delivery (n = 3,451). Supine and prone CT acquisitions
were obtained for all patients; right lateral decubitus series were obtained
in a minority of cases with overlapping regions of suboptimal distention on
both supine and prone views. No spasmolytics were given. Adequacy of colonic
distention was confirmed by an experienced CT technologist, and the acquired
imaging data were sent to the CTC workstation for postprocessing and
interpretation. In rare selected cases, the interpreting physician was
consulted to assess distention before the patient was taken off the table.
For the room air distention technique, a standard hand-held air bulb insufflator was connected to the rectal catheter via barium enema tubing. The CT technologist coached the patient on selfinsufflation. For patients who were unwilling or unable to perform self-insufflation, the technologist provided assistance as needed. Additional room air was generally added between supine and prone scanning, as tolerated by the patient.
For carbon dioxide distention, an automated delivery device was used (PROTOCO2L, E-Z-EM). Equilibrium pressure was generally set at 20–25 mm Hg, and carbon dioxide was delivered incrementally as follows: 1 L/min up to 0.5 L, 2 L/min from 0.5 to 1.0 L, and 3 L/min for volumes greater than 1.0 L. The delivery device contains an electronically controlled pressure relief valve set at 50 mm Hg and an independent redundant mechanical pressure relief valve set at 75 mm Hg. The luminal pressure was allowed to stabilize (typically, 1–3 minutes) before scanning. In our experience, peak pressures rarely if ever exceed 40 mm Hg. For the past few years, automated carbon dioxide delivery has been our standard first-line colonic distention technique, accounting for the greater number of cases with this method.
Testing for statistical significance in the difference in frequency of pneumatosis between room air and carbon dioxide distention techniques was performed using Fisher's exact test.
MDCT Protocol and CTC Interpretation
Single-breath-hold acquisitions were obtained on an MDCT scanner
(LightSpeed Series, GE Healthcare) with 1.25- to 2.5-mm collimation, 1-mm
reconstruction interval, 120 kVp, and 25–100 mAs or dose modulation
(Smart mA, GE Healthcare) with a noise index setting maximized at 50 and an mA
range of 30–300. CT data post-processing and interpretation were
performed using a commercial software system (V3D Colon, Viatronix). All CTC
studies were prospectively interpreted by an experienced gastrointestinal
radiologist. The window setting for polyp evaluation at 2D CTC consists of a
width of 2,000 H centered at 0 H for both the supine and prone data sets in
all cases. Because this display is sensitive for the detection of pneumatosis,
we believe that additional retrospective review to identify additional cases
of pneumatosis was not necessary because it would have been detected at the
prospective evaluation.
Positive Study Group
For the purposes of this study, the presence of abnormal extraluminal gas
detected at prospective CTC interpretation was the sole inclusion criterion.
For positive cases, the pertinent demographic data (age, sex, surgical
history), indication for CTC evaluation (screening vs diagnostic), colonic
distention technique (manual room air vs automated carbon dioxide), appearance
(linear vs cystic), and extent (segmental and circumferential involvement) of
pneumatosis at CT and on clinical follow-up (associated symptoms and
interventions) were reviewed. All patients were queried regarding clinical
status by telephone within 1–2 hours of completion of the CTC
examination. Additional review of the electronic medical record was also
performed to exclude the possibility of delayed effects related to the
pneumatosis.
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Pneumatosis involved the right colon in all patients (Figs.
1A,
1B,
2,
3A,
3B,
3C,
4A,
4B), including the ascending
colon in six, the cecum in five, and the proximal transverse colon in three.
The ileocecal valve itself was involved by submucosal gas in four patients
(Fig. 1A,
1B). The pneumatosis was
evident (at least in retrospect) on scout views in four patients (Fig.
3A,
3B,
3C). The appearance of
right-sided pneumatosis on cross-sectional CT images consisted of a relatively
thin curvilinear configuration, with variable extension around the short axis
of the colon (Figs. 1A,
1B,
2,
3A,
3B,
3C,
4A,
4B). Complete circumferential
involvement was present at least focally in four cases. No macrocystic changes
of typical pneumatosis cystoides coli were seen with right-sided pneumatosis.
In one case, however, more typical pneumatosis cystoides coli was present in
the left colon that was separate from the limited thin linear pneumatosis
present in the right colon (Fig.
4A,
4B). Because of its different
appearance and distribution, it is uncertain whether the left-sided
pneumatosis cystoides coli represented a preexisting condition. This patient
also had a 7-mm rectal polyp detected on CTC. Although the initial plan was to
have this patient undergo CTC surveillance, the patient ultimately underwent
optical colonoscopy 2 years later for polypectomy, at which time no definite
pneumatosis was identified. No significant polyps (i.e., 
6 mm) were
identified in the other five CTC patients with pneumatosis.
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No unexpected abdominal symptoms developed during CTC examination in any patient with pneumatosis. In fact, in the entire cohort of 5,368 adults, no significant complications were encountered that resulted in either hospitalization, intervention, or prolonged observation. To our knowledge, no delayed complications have developed in any patient. Immediate CTC follow-up in the six patients with colonic pneumatosis, which included at least a 2-hour interval, revealed that all six patients were asymptomatic after the procedure. None of the patients required clinical observation, intervention, or treatment of any kind. Long-term follow-up with a mean time interval of 19.2 months (range, 2–30 months) has revealed no negative delayed health effects related to the CTC procedure.
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Symptomatic perforation rates at optical colonoscopy typically range from 0.1% to 0.2% [4–10]. Barotrauma from pneumatic distention likely accounts for many of the right-sided colonic tears at colonoscopy, whereas left-sided perforations relate more to direct mechanical trauma from the endoscope [11]. Because CTC is a nontherapeutic evaluation, it is important for this procedure to show a safety profile that is far superior to that of colonoscopy. This is particularly the case if CTC is to be used for widespread screening of asymptomatic adults. From initial experiences with CTC, reported symptomatic perforation rates have varied from 0.03% to 0.005%, with nearly all cases of perforation involving manual staff-controlled room air insufflation in patients with significant underlying colorectal disease [12–14]. The risk of colonic perforation at asymptomatic CTC screening appears to be even lower and may approach zero when patient-controlled room air insufflation or automated carbon dioxide distention techniques are used [12].
In contrast to frank colonic perforation, we have encountered incidental right-sided pneumatosis at CTC with an overall frequency of approximately one case per 1,000. Detection of linear pneumatosis at CTC can be an un-settling finding for interpreting radiologists without extensive CTC experience. Although immediate and delayed follow-up is a prudent course of action that we continue to practice at our institution when pneumatosis is seen at CTC, we have learned to accept this as an incidental imaging finding in the absence of symptoms. Because the gas is extraluminal, we suspect that some of these cases of pneumatosis have been and will continue to be labeled by others as an "asymptomatic perforation" if this distinction is not recognized [12–14]. However, because of the innocuous clinical course of carbon dioxide–associated pneumatosis in our CTC series, we think that such terminology is inappropriate and would cause undue alarm, even in cases in which limited or borderline extramural extension of gas is present.
The excellent sensitivity of CT for detecting intraabdominal gas has raised the awareness of subclinical extraluminal gas related to colorectal evaluation, but this is not to say it is a new entity somehow unique to CTC [15, 16]. Because CT evaluation is not indicated for an asymptomatic patient after uneventful optical colonoscopy, the frequency of incidental extraluminal gas is not known. However, a recent study involving 118 failed colonoscopy examinations revealed unsuspected perforation at CT in two patients (1.7%), suggesting a role for low-dose CT evaluation immediately before colonic distention for CTC evaluation in this clinical setting (Kuntz MA et al., presented at the annual meeting of the Society of Gastrointestinal Radiologists, April 2007).
When extraluminal gas is detected at CTC examination, the key determinant for clinical management appears to be the presence or absence of symptoms. For gas limited to the intramural space (i.e., pneumatosis) in an asymptomatic adult undergoing CTC screening, our results suggest that this is an innocuous imaging finding for which no intervention or treatment is needed. Regardless, we still pursue short-term follow-up in these cases to confirm a benign clinical course. This approach may also apply to asymptomatic patients in whom pneumatosis is associated with limited, localized mesenteric extension of gas. With more extensive amounts of intraperitoneal or extraperitoneal extramural gas at CTC (which we have not yet observed), legitimate concern for frank perforation would exist and close clinical observation would be prudent, even in patients who are initially without symptoms.
The precise cause of asymptomatic pneumatosis at CTC is uncertain but likely is multifactorial. Factors that could conceivably be involved to varying degrees include issues of mucosal permeability and defects, intraluminal pressure and colonic wall tension, cathartic preparation, and even bacterial flora. Because colonic wall tension is proportional to the radius by Laplace's law, the more capacious right colon should be more susceptible to barotrauma at a given intraluminal pressure. Cadaveric studies have shown that pneumatosis caused by gaseous distention at colonoscopy can lead to serosal injury that generally precedes both mucosal and transmural rupture [17]. Even without frank perforation, areas of pneumatosis tend to involve the mesenteric side of the colon wall, which may explain the CT appearance in some of our patients with asymptomatic pneumatosis. With room air, the minimum intraluminal pressure resulting in serosal tearing was about 50 mm Hg [17], which is generally higher than the peak pressures achieved with the automated carbon dioxide technique at CTC. However, the increased permeability of carbon dioxide could conceivably allow pneumatosis at lower pressures, which may help explain why we have not encountered this finding at CTC with room air distention. Note that the peak intraluminal pressures seen at both optical colonoscopy and barium enema are significantly higher than seen at CTC with automated carbon dioxide delivery [17, 18]. It is quite possible that asymptomatic pneumatosis with these other colorectal examinations is underrecognized because there would be no clinical indication for pursuing CT.
Because the scout image for CTC is obtained after gaseous distention of the colon, we cannot definitively conclude that the cases of pneumatosis were caused by the carbon dioxide delivery. Even if the pneumatosis was not a preexisting condition, it is conceivable that another factor, such as the bowel preparation, contributed to its development. Although we were unable to find any reports linking cathartic bowel preparation with colonic pneumatosis, such purgation could perhaps prime the colon for pneumatosis by creating either small subclinical mucosal defects or permeability changes that could allow the passage of carbon dioxide, even under relatively low pressures.
In conclusion, asymptomatic right-sided colonic pneumatosis at CTC is a rare benign self-limited imaging finding. To date, we have seen this finding only with carbon dioxide distention, despite the fact that this technique generally results in lower peak intraluminal pressures than with manual room air distention. Although we recommend immediate clinical follow-up to confirm the lack of symptoms, this benign imaging finding should not be confused with frank perforation. The precise cause for the development of asymptomatic pneumatosis at CTC remains unclear, but we postulate a subclinical right-sided serosal defect (either preexisting or created) coupled with the increased permeability of carbon dioxide relative to room air.
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