The technical objective of computed tomographic colonography (CTC) is to acquire high-quality computed tomography images of the cleansed, well-distended colon for polyp detection. In this article the authors provide an overview of the technical components of CTC, from preparation of the patient to acquisition of the imaging data and basic methods of interpretation. In each section, the best evidence for current practices and recommendations is reviewed. Each of the technical components must be optimized to achieve high sensitivity in polyp detection.
As early as 1983, Computed tomography (CT) was recognized as a potential colon cancer screening technique. By 1994, technological advances allowed realization of what is now called CT colonography (CTC) or virtual colonoscopy. The technical objective of CTC is to acquire high-quality CT images of the cleansed, well-distended colon for polyp detection. Since the mid 1990s, many studies have confirmed the ability of CTC to accurately detect polyps and colorectal cancer. and there exist well over 1000 peer-reviewed articles on various aspects of CTC. The ultimate clinical implementation of CTC, however, continues to be controversial, most recently manifest in the fierce debate over Medicare coverage.
In this article the authors provide an overview of the technical components of CTC, from preparation of the patient to acquisition of the imaging data and basic methods of interpretation. In each section, the best evidence for current practices and recommendations is reviewed. Each of the technical components must be optimized to achieve high sensitivity in polyp detection. That being said, the tremendous research and technical advances that have occurred over the last decade should now enable any modern CT imaging center to perform high-quality examinations.
Bowel preparation
Background
Adequate bowel preparation may be even more critical for CTC than for colonoscopy. Whereas in colonoscopy, rinsing and suction may be used to remove residual stool and/or liquid, there is no such opportunity to alter the colonic contents once the CTC images have been acquired. Imaging the patient in both supine and prone positions is helpful, but does not substitute for an adequate preparation. Adherent stool is the most common cause of false-positive findings on CTC. Retained liquid and stool can also obscure lesions, especially small ones, resulting in false-negative diagnoses. Interpretation times also increase when a large number of false lesions must be interrogated and documented.
Diet
Dietary restriction is a prerequisite to a good pharmacologic bowel preparation, and should begin at least 1 day before CTC. Low-residue solids may be consumed that morning, followed by a purely liquid diet the remainder of the day. It is important to avoid high residue foods and dairy products.
Pharmacologic Laxatives: Wet and Dry
There is a multitude of pharmacologic colon cleansing preparations, reflecting the difficulty in perfecting one that balances strength with safety, taking into account patient acceptance and tolerance. Among those available, the major distinction lies between so-called dry preps and wet preps.
Dry prep
The central ingredient of a dry prep usually consists of a low-volume, hyperosmotic preparation with either sodium phosphate (NaP) or magnesium citrate. The dry preps cause an osmotic catharsis as intraluminal saline draws plasma water into the bowel lumen. Macari and colleagues reported that on average, a phospho-soda preparation provided significantly less residual fluid than a polyethylene glycol preparation, which is advantageous in CTC.
Sodium phosphate
Oral NaP products include the prescription products Visicol and OsmoPrep, and over-the-counter laxatives (eg, Fleet Phospho-soda). The liquid form is packaged in a 45-mL bottle, which is mixed with 4 ounces of water and taken late in the afternoon with 8 additional ounces of water on the day before CTC. The taste is considerably salty. Onset to catharsis is approximately 1 hour. Four bisacodyl tablets are also taken orally in the evening after the NaP is finished, and a bisacodyl rectal suppository is inserted the morning of the examination. Some have advocated double dose (90 mL) of NaP, but a single dose is just as effective. NaP also comes in pill form. The tablet-based formulation bypasses the problem of flavor and also enables oral intake with any clear liquid.
The routine use of NaP is controversial due to its history of causing serious electrolyte abnormalities. Patients may become dehydrated and develop hyperphosphatemia, hypocalcemia, hypernatremia, and hypokalemia. Metabolic acidosis, tetany, and death have been reported. In addition, rare reports of acute phosphate nephropathy have been published. Acute phosphate nephropathy is associated with calcium-phosphate crystal deposition in the renal tubules that may result in permanent renal dysfunction, sometimes requiring dialysis. The risk appears to be related to factors such as advanced age, hypovolemia, baseline renal insufficiency, increased bowel transit time, colonic mucosal injury from colitis, or the use of nephrotoxic medications such as diuretics, angiotensin-converting enzyme inhibitors, angiotensin receptor blockers, and possibly nonsteroidal anti-inflammatory drugs (NSAIDs). As such, the Food and Drug Administration (FDA) has required the manufacturer of Visicol and OsmoPrep to add a Boxed Warning to their labeling.
A 2008 review by Belsey and colleagues analyzed all available published sources of adverse events reported for both NaP and polyethylene glycol (PEG). These investigators highlighted a 1998 meta-analysis of 8 trials investigating the adequacy of NaP versus PEG preparation for optical colonoscopy. The quality of cleansing was similar, but NaP was superior in terms of patient tolerance and cost. Another meta-analysis, looking at 16 studies, also demonstrated superiority of NaP. However, the largest meta-analysis, based on 24 studies, showed no significant difference between NaP and PEG. None of the 3 meta-analyses demonstrated any significant difference in adverse events. In fact, in the largest analysis neither group suffered any clinically significant serious adverse events. Some CTC programs have screening questionnaires to triage at-risk patients away from NaP. However, such systems are imperfect, as one study showed that 2% of cases with contraindication to NaP could not have been prospectively excluded based on their clinical history alone. Many CTC programs have thus decided to terminate its use. If used, however, the manufacturers have advised that the dose be restricted or split and that the patient drink sufficient liquids.
Magnesium citrate
Magnesium citrate can be dispensed in powder or liquid form. The powder form is mixed with 16 ounces of liquid. The liquid form comes ready to drink in a 10-ounce bottle. Like NaP, magnesium citrate is taken in the late afternoon 1 day before the examination. Time to onset of catharsis is around 1 hour. Oral hydration should be maintained to prevent dehydration.
As with NaP, bisacodyl tablets are taken the night before, and a bisacodyl suppository on the morning of the examination. The sodium content of magnesium citrate is much less than NaP and therefore may be preferred in patients at risk for electrolyte abnormalities. In a 2005 study by Delegge and Kaplan, 506 patients undergoing optical colonoscopy were randomized to receive either a magnesium citrate (LoSo Prep, containing magnesium citrate, bisacodyl tablets and a bisacodyl suppository) or NaP-based prep (double dose NaP). The group that received magnesium citrate demonstrated superior colon cleansing, and frequency of reported side effects was similar for both groups (59% vs 58% for NaP and Neutra prep/LoSo prep, respectively).
Wet prep
A wet prep refers to a high-volume, iso-osmotic preparation based on PEG. PEG is a washout lavage preparation that is nonabsorbable and is osmotically balanced. PEG does not cause fluid shifts from the intracellular to the extracellular space. A disadvantage of this preparation is considerable residual fluid in the colon, which is easily suctioned at optical colonoscopy but obscures portions of the bowel wall in CTC ( Fig. 1 ).
PEG
Standard preparation with PEG is usually accomplished by drinking 4 L of the solution the afternoon before the examination. Although popular for colonoscopy preparation, PEG has progressively fallen out of favor for use in CTC, for both technical and patient-related reasons. A PEG preparation not infrequently leaves liquid in the colon, potentially obscuring lesions. PEG also has the poorest adherence of the preparations, due to its consistency and taste as well as the imposing volume. At one experienced center, PEG accounts for less than 1% of CTC preparations. However, PEG does have the advantage of not causing fluid shifts and is safe for those in fragile health. Trials examining the relative efficacies of NaP versus PEG have yielded varying results. A 2009 Japanese study compared the performance and safety of the NaP tablet (with and without laxatives) and PEG bowel preparations prior to colonoscopy, and found the quality of colon cleansing equivalent. Although serum levels of inorganic phosphorus were abnormally increased in the NaP groups, these increases were only transitory. A study performed on a population with a high-residue diet showed better colonic cleansing and shorter CTC interpretation times with a PEG-based preparation compared with the NaP-based preparation.
Side effects associated with PEG are not as alarming, but data suggests that it too is potentially associated with electrolyte disturbances, albeit to a lesser extent than with NaP. Reported adverse events attributable to oral PEG generally reflect sodium imbalance, gastrointestinal injury caused by vomiting, allergic reactions, and aspiration. Regardless of the type of bowel preparation, the majority of patients experience discomfort and inconvenience. Ongoing research to perform low-prep or no-prep CTC with fecal tagging has the potential to eliminate the most onerous part of the examination.
Fecal Tagging
Background
Many CTC programs now routinely employ fecal tagging. Fecal tagging refers to the oral ingestion of high-density oral contrast agents so that residual colonic contents, liquid and solid, are homogeneously high in attenuation and can therefore be differentiated easily from soft tissue density polyps ( Fig. 2 ). Tagging may therefore help improve the performance of CTC for polyp detection. Many different contrast agents and combinations of agents have been used for fecal tagging. In general, there are 2 main classes in common use: barium-based and iodine-based (both ionic and nonionic).
Barium
Many different densities of barium-based tagging agents have been proposed, and tagging protocols using barium alone have been reported to be effective. Barium-based formulations (eg, Tagitol V 40% w/v) are similar to those regularly used in standard abdominal CT scanning, have an excellent safety record, and are familiar to radiologists. There is some evidence that barium selectively adheres to polyps with villous histology, which may prove beneficial in polyp diagnosis. On the other hand, high-density barium, particularly if the density is heterogeneous, produces problems for electronic cleansing regimens, discussed later. In addition, barium can cause constipation or even impaction.
Iodinated
Iodine-based agents are similarly safe and familiar. Studies have demonstrated that iodinated contrast ingested alone may also be used to tag residual material in the colon. Iodinated agents are hypertonic, can cause fluid shifts into the bowel lumen, and thus have an additional cathartic effect. In a 2009 retrospective study of nonlaxative or minimum-laxative regimens, Nagata and colleagues found the homogeneity of tagged fecal matter was better with iodine-based regimens then with barium.
Ionic iodinated
Iodinated contrast agents come in 2 varieties, ionic and nonionic. Both are water soluble, which promotes more homogeneous tagging. Diatrizoate meglumine and diatrizoate sodium (Gastrografin 37% organically bound iodine) is an ionic iodinated contrast agent that is commonly used as oral contrast in standard CT examinations, as well as for fluid/stool tagging in CTC ; it is less expensive than nonionic. However, the taste is not palatable, especially when drinking large amounts. Although oral ionic iodinated contrast agents are generally safe, they can induce gastrointestinal complaints and dehydration, and rare anaphylactic reactions have been reported. Sodium diatrizoate is contraindicated in those with iodine allergies. Doses as low as 20 mL of been shown to be adequate for tagging purposes.
Nonionic iodinated
Nonionic iodinated contrast (ie, iopromide, iohexol) has a low risk for causing dehydration and diarrhea. Unlike sodium diatrizoate, it is almost tasteless and has good patient acceptance. However, this contrast agent is more expensive than both barium and ionic iodinated contrast.
Of course, the use of barium and iodine-based tagging agents are not mutually exclusive. The strategy behind combined tagging is to achieve opacification of residual solids with barium, and of fluid with iodine. These agents have been successfully used in combination, as was done in the multicenter ACRIN National CT Colonography Trial. A total volume of 40 mL of 40% w/v barium (Tagitol V) was administered orally the day before the CT scan in 3 divided doses. A total volume of 60 mL of sodium diatrizoate was administered in 3 doses of 20 mL starting the evening before the CT scan.
Although there is no consensus regimen, the European Society of Gastrointestinal and Abdominal Radiology suggests that the choice of tagging agent should be based on local experience, taking into account any history of allergy.
Limited prep and noncathartic CTC
Preparation is one of the most unpleasant aspects of CTC, and patients would have the examination more frequently if bowel preparation was not required. Interest in developing tagging regimens is rooted in improving patient experience and compliance by decreasing or eliminating the need for a cathartic. Noncathartic or reduced cathartic CTC is more tolerable, especially for those with impaired mobility or those who have a poor response to laxatives. Polyp detection in noncathartic or reduced cathartic preparations with fecal tagging is an area of intense ongoing research, with early studies reporting encouraging results.
In a 2008 study of 40 patients who underwent the same fecal tagging regimen before CTC, the patients were randomized to 4 different cathartic regimens of varying intensity. There was no difference in image quality between the different cathartic groups. Bisacodyl, 30 mg and magnesium citrate, 16.4 g did not provide better image quality than bisacodyl alone, 20 mg. Patient acceptance rates were lower in the more aggressive cathartic groups.
In a 2008 study by Jensch and colleagues, CTC with fecal tagging without stool subtraction and a bisacodyl-only prep was compared with colonoscopy. Despite homogeneous fecal tagging, there was a large number of false-positive findings (specificity 79%) when 6 mm was used as a size threshold. In a 2009 study by Nagata and colleagues, minimum laxative fecal tagging CTC demonstrated equally high sensitivity to full laxative examination. However, the full laxative fecal tagged CTC yielded a higher specificity. The investigators concluded that it might be desirable to offer patients the option of the full prep for highest accuracy and the ability to perform a same-day colonoscopy, or a minimum laxative CTC for those willing to accept an increased risk of false positives and attendant unnecessary colonoscopy, which not only is inconvenient, but increases risk and costs.
Electronic Subtraction of Tagged Material
“Electronic cleansing” or “electronic subtraction” of fluid and fecal contents is an area of active research, with the goal of manipulating the images such that the high-density tagging material is removed, but without interfering with polyp detection. This manipulation is important for visualization as well as for computer-aided polyp detection, whether the prep is a full prep with fecal tagging or a less rigorous limited or noncathartic one. Several commercial platforms now employ algorithms for electronic cleansing. At present, electronic subtraction is technically challenging, principally because of heterogeneous fecal tagging, variable colonic transit times, and normal stool desiccation as it progresses toward the rectum. Also, interfaces of stool, air, and tissue are prone to partial volume artifacts. “Oversubtraction,” where normal tissue or polyps are subtracted along with stool, must be avoided. Although stool subtraction has been shown to improve sensitivity of CTC, studies have also shown that the specificity can decrease, especially for the detection of moderate-sized polyps.
One of the main issues with noncathartic preps is difficulty in performing a primary 3-dimensional (3D) interpretation without the ability to perform electronic cleansing. Residual stool and artifacts render the 3D virtual colonoscopic view unreadable, as the colonic mucosa is essentially “buried.” A large number of filling defects would have to be addressed one by one. Even with stool subtraction, optimal fecal tagging would be needed to make 3D interpretation possible. Without stool subtraction, a primary 2-dimensional (2D) method must be employed with 3D problem solving. A primary 2D approach permits the reader to quickly examine the internal density of filling defects and decide if they are truly soft tissue polyps or if they contain air or tagging agent consistent with stool.
As part of a 2006 study by Zalis and colleagues, a group of CTC patients who ingested magnesium citrate preparation and iodinated fecal tagging agent without dietary restriction were compared with a group of patients who took PEG prep with standard dietary restrictions. Electronic subtraction was applied. Readability was equal between the 2 groups, and discomfort was less in the magnesium citrate group. In a 2008 study of a group of patients drawn from the Walter Reed Army Medical Center public database, Serlie and colleagues found that electronic cleansing shortened interpretation time, lowered assessment effort, and had a positive effect on observer confidence.
Same-Day CTC and Colonoscopy Service: Impact on Selection of Bowel Prep
In an ideal setting, positive CTC examinations could be followed up with same-day colonoscopy, thereby avoiding a second bowel cleansing for the patient. This procedure requires close coordination with the gastroenterology department at each particular institution. Patients should be scheduled for CTC in the early morning while their colon remains freshly prepared. For appropriate triage, the studies need to be interpreted within 1 to 2 hours following data acquisition, while the patient remains NPO (nil by mouth) and awaits further instructions. Positive findings can then be communicated directly to the patient and to the gastroenterologist. Some flexibility in the colonoscopy schedule is needed so that CTC patients can be accommodated when needed. The amount of flexibility is determined by the work flow of the CTC program as well as the referral rate. The referral rate is in turn determined by the size threshold for referral. This threshold must be chosen in consultation with the local gastroenterologists. For example, if a size threshold of 5 mm is chosen for referral to colonoscopy, more patients will be referred than if the threshold were 1 cm.
The issue of patient preparation must also be addressed by consensus. The preparation for CTC must be acceptable to the gastroenterologist as adequate for colonoscopy. In some instances, as in a 2002 study by Lefere and colleagues, additional preparation is performed between CTC and colonoscopy. In that study, a preparation regimen of magnesium citrate and fecal tagging agents was compared with PEG solution without fecal tagging. Because the preparation for CTC was less aggressive, patients underwent additional colonic cleansing with PEG before colonoscopy. The time between CTC and colonoscopy was 2 to 3 hours. Patients who get their CTC with the option of same-day colonoscopy must adhere to guidelines intended for colonoscopy patients, who are prepared for potential polypectomy; this includes stopping aspirin and NSAIDs. The images of the CTC should be available to the gastroenterologist, in a format which is intuitive and informative. Polyp size, location, and distance from the rectum should be easily attainable ( Fig. 3 ). 3D endoluminal and “virtual barium enema” ( Fig. 4 ) are excellent views to include. These images can be reconstructed on a 3D workstation and either sent back to PACS (picture archiving and communications system) or be made available on the 3D server.
Bowel insufflation and spasmolytics
Patient Arrival
The patient arrives in the CT suite approximately 2 to 3 hours after completion of the bowel preparation, at a time when evacuation of as much residual liquid as possible has been achieved. The technologist inquires about compliance with the preparation as well as appearance of the stool. If the patient has not finished the preparation or is continuing to have semisolid stools, rather than rescheduling the examination, more cathartic agents may be administered in the department. Before the examination, the patient is encouraged to use the restroom one last time.
Insufflation
Adequate colonic distention is of fundamental importance for CTC. Collapsed bowel segments may reduce sensitivity and specificity, obscuring disease or mimicking pathology. Diagnostic confidence can be reduced and interpretation times increased. Distention can be achieved by staff or patient administration of either room air or carbon dioxide (CO 2 ), via a manual pump or electronic insufflator. The simplest and least expensive technique is room air insufflation using a hand-held plastic bulb. This method can even be performed by patients themselves. Of the possible combinations, electronic insufflation of CO 2 is favored for the reasons given below.
Burling and colleagues demonstrated that automated CO 2 insufflation significantly improved colonic distention compared with manual CO 2 insufflation for CTC, particularly the left colon in the supine position and the transverse colon when both supine and prone scans were combined. Slow administration of CO 2 at continuous low pressures likely decreases colonic spasm, especially in segments with diverticular disease ( Fig. 5 ). CO 2 is, because of its superior lipid solubility and higher partial pressure gradient, more rapidly absorbed by the colon than room air. Thus, compared with room air, postprocedural gaseous discomfort is reduced. Complications are also likely reduced, as close to all of the reported perforations from CTC have involved staff-controlled manual insufflation of room air. The perforation risk with electronic CO 2 insufflation is negligible in the screening population.
A physician, radiology technician, or nurse inserts a thin, flexible rectal catheter that is connected to the electronic CO 2 insufflator (PROTOCO2L; Bracco Diagnostics, Princeton, NJ, USA). Larger catheters, such as those used at barium enema, are not typically used unless the patient has difficulty retaining the gas. The balloon may or may not be inflated. The target pressure, usually around 25 mmHg, is programmed and the CO 2 is insufflated, titrating to pressure and patient comfort. Because of differences in colonic anatomy, patient tolerance, ileocecal reflux, and anal incontinence, the total volume of CO 2 delivery can vary a great deal, and thus has little significance. Anywhere from 3 to 10 L may be needed for adequate distention. Cooperation with gas retention is essential.
Insufflation techniques vary between centers, but often start with the patient in the right-side down decubitus position to facilitate rectosigmoid and descending colon distention. Insufflation is continued in the supine position until the patient reports fullness in the right side of the abdomen, usually indicating cecal distention. It is crucial to acquire the CT images during active replacement of CO 2 at equilibrium pressures. A scout radiograph is then used to assess colonic distention ( Fig. 6 ). If adequate, supine CT images are obtained. The scout, however, is sometimes unreliable for evaluation of distention. At some institutions technologists or research assistants are trained to assess the adequacy of distention by reviewing the CT images on the scanner console. This assessment allows for problem solving in real time, and reduces the need for callbacks.
After supine acquisition, the patient is then turned prone and the scout is then repeated. More CO 2 may or may not need to be insufflated. Elevation of the torso and hips with pillows, especially in overweight patients, can improve distention of the transverse colon. Axial prone images are then obtained. The supine and prone scans are obtained at end expiration, elevating the diaphragm, and allowing more room for the splenic flexure and transverse colon. The rationale of dual positioning is to redistribute residual fluid and as well as to help redistribute air ( Fig. 7 ). Polyp detection sensitivity has been proven to improve when both supine and prone acquisitions are performed ( Fig. 8 ).
Glucagon
Some investigators have studied spasmolytic agents such as glucagon with the goal of reducing bowel peristalsis and resulting motion artifact. Part of the justification for using glucagon in CTC arises from its role as an antiperistaltic agent in barium enema studies. The data regarding glucagon’s efficacy in colonic radiology is conflicting. Lappas and colleagues, in a placebo-controlled study of glucagon effects in patients having double-contrast barium enemas, demonstrated that glucagon improved patient discomfort. However, an effect was not noted until after 8 minutes post administration. On a practical level, because of the speed of the CTC, patients will have already completed the examination before glucagon achieves its maximum effect. Moreover, waiting for maximum effect increases duration of the CTC examination and decreases efficiency. Other studies of glucagon have shown no beneficial effect. Yee and colleagues performed a blinded, nonrandomized study of 60 patients undergoing CTC. The 33 patients who were administered glucagon did not show any difference and segmental or overall colonic distention. Morrin and colleagues studied 74 patients who were administered glucagon before CTC and found that distention scores for the glucagon and nonglucagon patients were similar. In addition, Glucagon is costly (wholesale cost is US$48–66 per 1-mg vial) and requires an intravenous or intramuscular injection. Also, glucagon carries a risk of side effects.
Glucagon’s lack of proven effectiveness in CTC is not surprising from a physiologic standpoint, given that the colon is recognized as the least responsive part of the bowel to the antiperistaltic effects. Thus, routine administration of glucagon is not recommended. However, glucagon may be given in the setting of significant abdominal discomfort or if there is persistent spasm or poor distention not improved by dual positioning.
Though not available in the United States, the spasmolytic hyoscine- N -butylbromide (Buscopan) is available in Europe, and has been suggested to be more effective than glucagon as an antiperistaltic agent. However, despite improved colonic distension in certain segments, Buscopan did not necessarily translate into improved polyp detection, thus is not routinely used in CTC.
Based on the literature and personal experience, there does not appear to be justification for routine use of spasmolytics in CTC. At the same time, a small percentage of patients may have cramping and pain that significantly limit tolerance of bowel insufflation, and in these cases ad hoc administration of glucagon may be worthwhile.
Bowel insufflation and spasmolytics
Patient Arrival
The patient arrives in the CT suite approximately 2 to 3 hours after completion of the bowel preparation, at a time when evacuation of as much residual liquid as possible has been achieved. The technologist inquires about compliance with the preparation as well as appearance of the stool. If the patient has not finished the preparation or is continuing to have semisolid stools, rather than rescheduling the examination, more cathartic agents may be administered in the department. Before the examination, the patient is encouraged to use the restroom one last time.
Insufflation
Adequate colonic distention is of fundamental importance for CTC. Collapsed bowel segments may reduce sensitivity and specificity, obscuring disease or mimicking pathology. Diagnostic confidence can be reduced and interpretation times increased. Distention can be achieved by staff or patient administration of either room air or carbon dioxide (CO 2 ), via a manual pump or electronic insufflator. The simplest and least expensive technique is room air insufflation using a hand-held plastic bulb. This method can even be performed by patients themselves. Of the possible combinations, electronic insufflation of CO 2 is favored for the reasons given below.
Burling and colleagues demonstrated that automated CO 2 insufflation significantly improved colonic distention compared with manual CO 2 insufflation for CTC, particularly the left colon in the supine position and the transverse colon when both supine and prone scans were combined. Slow administration of CO 2 at continuous low pressures likely decreases colonic spasm, especially in segments with diverticular disease ( Fig. 5 ). CO 2 is, because of its superior lipid solubility and higher partial pressure gradient, more rapidly absorbed by the colon than room air. Thus, compared with room air, postprocedural gaseous discomfort is reduced. Complications are also likely reduced, as close to all of the reported perforations from CTC have involved staff-controlled manual insufflation of room air. The perforation risk with electronic CO 2 insufflation is negligible in the screening population.
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