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European Journal of Radiology 82 (2013) 1137– 1143

Contents lists available at SciVerse ScienceDirect

European Journal of Radiology

jo ur nal ho me page: www.elsev ier .com/ locate /e j rad

owel preparation for CT colonography

manuele Neria,∗,1, Philippe Lefereb, Stefaan Gryspeerdtb, Pietro Bemia,nnalisa Mantarroa, Carlo Bartolozzia

Diagnostic and Interventional Radiology, University of Pisa, ItalyDepartment of Radiology, Stedelijk Ziekenhuis, Roeselare, Belgium

a r t i c l e i n f o

rticle history:eceived 29 October 2012ccepted 5 November 2012

eywords:T colonography

a b s t r a c t

Bowel preparation represents an essential part of CT colonography, as the accuracy of the exam is stronglyrelated to the adequacy of colonic cleansing, and a poor bowel preparation may compromise the diag-nostic quality even despite optimization of all other acquisition parameters. Residual stool and fluid inthe large bowel may affect the interpretation of the exam and may increase the number of false positivesand false negatives. In this regard, the majority of patients having undergone CT colonography state that

owel preparationolon

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bowel preparation is the most unpleasant part.Unfortunately, to date no definite consensus has been reached about the ideal bowel preparation

technique, and there is great variability in preparation strategies across diagnostic centers.The purpose of this review article is to describe the development and evolution of bowel preparation

techniques in order to choose the best approach for optimizing the diagnostic quality of CT colonographyin each patient.

. Introduction

Bowel preparation represents an essential part of CT colonogra-hy, as the accuracy of the exam is strongly related to the adequacyf colonic cleansing, and a poor bowel preparation may compro-ise the diagnostic quality even despite optimization of all other

cquisition parameters. Residual stool and fluid in the large bowelay affect the interpretation of the exam and may increase the

umber of false positives and false negatives. In fact, retained stoolan mimic polyps, thus decreasing specificity, whereas retaineduid can obscure them, resulting in lower sensitivity [1].

Moreover the quality of acquisition, and the accuracy of repor-ing, depend on radiologist’s skills, successful bowel preparationelies mainly on patient compliance. To this respect, the majorityf patients having undergone CT colonography state that bowelreparation is the most unpleasant part [2].

Unfortunately, to date no agreement has been reached about the

deal bowel preparation technique, and there is great variability inreparation strategies across diagnostic centers [3].

∗ Corresponding author at: Diagnostic and Interventional Radiology, Departmentf Traslational Research and New Technologies in Medicine and Surgery, Universityf Pisa, Italy.

E-mail address: emanuele.neri@med.unipi.it (E. Neri).1 Nuovo Ospedale S. Chiara, UO Radiodiagnostica 1, Via Paradisa 2, 56100 Pisa,

taly.

720-048X/$ – see front matter © 2012 Elsevier Ireland Ltd. All rights reserved.ttp://dx.doi.org/10.1016/j.ejrad.2012.11.006

© 2012 Elsevier Ireland Ltd. All rights reserved.

The review article describes the development and evolution ofbowel preparation techniques for CT colonography.

2. Bowel preparation

Protocols for bowel preparation are extremely variable because,in the early years of CT colonography, different groups ofresearchers used protocols derived from double-contrast bariumenema or conventional colonoscopy, according to local practices.However, all preparation schemes were at that time composed oftwo basic steps [4]:

(1) a low-residue diet;(2) the administration of laxative drugs.

3. Low-residue diet

In all bowel preparation schemes, a low-residue diet is recom-mended starting a few days before CT colonography in order tolimit the intake of slowly absorbed or non-absorbable food (suchas vegetable) that would remain in the large bowel at the time ofthe exam, thus potentially mimicking or hiding parietal lesions. Thelow-residue diet lasts for a period from one to five days, with mostcenters prescribing a diet of 1–3 days. However, evidence exists that

low-residue diet could even be avoided, as it does not seem to sig-nificantly affect proper intestinal cleansing [5]. Yet, patients withchronic constipation are suggested to increase their fiber intakein the days before CT colonography so to reduce intestinal transit

1 l of Radiology 82 (2013) 1137– 1143

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Fig. 1. (a) Preparation regimen with PEG as cleansing agent (“wet” preparation), andno tagging. In the prone decubitus, untagged fluid is stratified along the transversecolon (arrow) and masks the colonic wall (arrowheads) where parietal lesions could

138 E. Neri et al. / European Journa

ime, thus favoring complete colonic cleansing [6]. Therefore theiet restriction can be changed accordingly to patient’s bowel habit.

. Cathartic-only approach

The cathartic-only approach was the most widely used prepa-ation technique at the early days of CT colonography. It is derivedrom the preparation schemes used for conventional colonoscopynd its aim is to achieve strong colonic purgation by means ofathartic agents. This technique allows a good visualization ofhe colonic walls whenever optimal colonic cleansing is obtained;owever, the diagnostic quality of the examination is usually com-romised if purgation is not effective, due to the difficulty ofifferentiating colonic polyps from stool residues. In real practice,ptimal colonic cleansing with no residual stool is very hard tobtain. Although polyps can usually be differentiated from fecal oruid residues based on their fixity to the colonic wall; small fecalesidues may as well remain fixed to the bowel wall in both theupine and prone position, potentially resulting in false positivendings. Conversely, fluid residue may obscure small polyps, thuseducing sensitivity [1]. For this reason, research had previouslyocused on the use of cathartic agents that allowed to minimizeesidual fluid, resulting in a relatively “dry prep”. Besides, the issuef fluid residue has become of less concern with the more recentntroduction of fecal and fluid tagging protocols, as described in aater section.

Another drawback of cathartic-only preparations is poor patientompliance. While most patients prefer CT colonography overonventional colonoscopy [9], the majority of those who havendergone CT colonography state that bowel preparation is theost unpleasant part of the examination. Research is therefore

imed at developing less invasive preparations (so-called “reduced-athartic”) or even eliminating the need for bowel preparation atll (“prep-less” approach) [8–12].

. PEG

Polyethylene glycol electrolyte (PEG) is the most effectiveleansing agent for conventional colonoscopy, as well as the laxa-ive drug most widely used at the beginning of the CT colonographyra. It is a hydrophilic, non-absorbable iso-osmolar solution thatauses an intense watery diarrhea without affecting electrolytealance [13]. For CT colonography purposes, PEG-based prepara-ions are called “wet” because they leave a significant amount ofesidual fluid in the large bowel, that may substantially cover theolonic endoluminal surface, thus potentially reducing sensitivityn detection of colonic lesions [14] (Fig. 1a). However, PEG has thedvantage of having a quick laxative action with few side effects,ince it does not alter the patient’s electrolyte balance. Therefore,EG is safe especially in elderly patients or in those in poor gen-ral condition. Conversely, its main contraindications are paralyticleus, gastric retention, gastrointestinal obstruction, bowel perfo-ation, toxic colitis, and toxic megacolon [15]. In addition, the higholume (up to 4 L) of PEG solution to be ingested before CTC and itsalty taste make it poorly tolerated by a large number of patients;oreover, mild but still unpleasant symptoms commonly occur

fter PEG administration, such as abdominal discomfort, bloating,ausea, and vomiting [16].

In a work by Hookey et al., 40% of patients were unable to com-lete the preparation with PEG. This latter was tolerated by 33%f patients, while 84% of them preferred a sodium phospate-based

reparation protocol [17].

To alleviate these problems, gastroenterologists have pro-osed an alternative schedule of PEG administration for opticalolonoscopy, based on the ingestion of only 2 L of PEG; volume

be missed. (b) Preparation regimen with sodium phosphate as cleansing agent (“dry”preparation), and no tagging. Untagged solid residues (arrowheads) may remainadherent to the colonic wall and be difficult to distinguish from polyps.

reduction is made possible by associating bisacodyl, a contactlaxative that induces peristalsis by acting locally on the parasympa-thetic system. A study comparing the full volume (4 L) PEG prepa-ration and the reduced volume (2 L), combined PEG + bisacodylscheme showed better patient acceptance of this latter (93% vs.66%) with comparable quality of colonic cleansing [18].

6. Sodium phosphate

Sodium phosphate is an oral saline laxative widely used forpatient preparation for barium double-contrast barium enema andoptical colonoscopy. It is a non-absorbable, osmotically active inor-ganic salt that leads to inversion of the normal water flow throughthe bowel wall, causing more fluid to enter the colonic lumen thancan be absorbed by the mucosa. In addition, sodium phosphatestimulates peristalsis, resulting in faster intestinal transit [19].

There are essentially two different patterns of preparation,based respectively on the administration of a single 45-mL dose(generally combined with bisacodyl) or a double, 90-mL dose ofsodium phosphate. Although preferred by some gastroenterolo-gists, this latter is now almost no longer used for CT colonography,because it does not significantly improve colonic cleansing [20].

Bowel preparation with sodium phosphate is defined as dry,

because the amount of residual fluid in the colonic lumen islower than PEG-based preparations. This is particularly importantbecause, unlike in optical colonoscopy, intraluminal fluid cannot beaspirated in CT colonography .

E. Neri et al. / European Journal of Radiology 82 (2013) 1137– 1143 1139

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Fig. 3. (a) Preparation regimen with barium. The head (arrowhead) and pedicle(arrow) of a pedunculated polyp of the sigmoid colon are partially covered by a thin

tered in 2 sachets of 15.08 g to be dissolved each in one glass of

ig. 2. Preparation regimen with barium. Barium tagging provides a complete solidtool with high-attenuation of solid fecal residual and facilitates the differentiationrom polyps.

Compared with PEG, sodium phosphate allows a substantialeduction of residual colonic fluid and is more tolerated, owingo the lower volume of solution to be ingested and to its betteraste [14]. However, a dry colonic preparation may also lead toersistence of solid fecal residues, which remain adherent to theolic walls and may mimic small polyps (Fig. 1b). This is espe-ially true if the patient has not strictly followed the prescribedow-residue diet; in this latter case, PEG-based preparations tendo be better in terms of image quality and diagnostic accuracyor identification and characterization of small polyps [20,21].

oreover, sodium phosphate may lead to a rapid increase inerum sodium concentration with the risk of hypokalemia, hyper-hosphatemia (up to 39% of patients) and hypocalcemia (5% ofatients) [22]. Therefore, sodium phosphate is contraindicated inatients with congestive heart failure or renal failure. To this lat-er respect, in May 2006 a FDA warning was issued about thenset of acute phosphate nephropathy following oral intake ofodium phosphate as a part of a bowel preparation scheme [23].lthough very rare, acute phosphate nephropathy can lead to per-anent renal failure that may require treatment with chronic

ialysis.

. Magnesium citrate

Magnesium citrate is another saline laxative with an actionimilar to that of sodium phosphate, which promotes fluid accu-ulation in the large bowel due to its osmolarity and stimulates

eristalsis. The laxative action is obtained in a few hours afterngestion. As with sodium phosphate, colonic cleansing achieved

ith magnesium citrate is dry, as only a small amount of resid-al fluid is left in the colonic lumen. However, magnesium citrateas a better safety profile than sodium phosphate, because sys-emic hydro-electrolyte balance is less affected and the risk ofevere hydro-electrolytical disturbances is negligible. Nonethe-ess, caution is still recommended in patients with renal failure24].

Magnesium citrate is available as an aqueous solution or as aowder, and can be administered in combination with bisacodyl.he rationale for this latter preparation is to cleanse the colonith magnesium citrate, while bisacodyl helps remove small fecal

film of contrast. (b) Preparation regimen with barium. A sessile polyp (arrow) in thedescending colon, is surrounded by a dense and homogeneous film of barium.

residues from the proximal colon and empty the distal colon. Verypopular in the United States, magnesium citrate is unfortunatelynot commercially available in Europe.

8. Sodium picosulphate

A very good alternative is sodium picosulphate. Besides being asmooth and dry cathartic, sodium picosulphate is widely availablethroughout Europe. Sodium picosulphate is a stimulant laxative.It is administered in a low volume and has a laxative effect byincreasing luminal fluid and enhancing peristalsis. It is adminis-

water. Sodium picosulphate is contraindicated in cases of severerenal insufficiency and congestive heart failure. Causing less sideeffects, it is smoother than sodium phosphate and is hence moreattractive to prepare the patient for CT colonography [25].

1140 E. Neri et al. / European Journal of Radiology 82 (2013) 1137– 1143

Fig. 4. Preparation regimen with same-day iodine oral administration. CTC in supine (a and c) and prone (b and d) decubitus obtained three hours after the oral intake of1 g is as the s

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00 mL of Gastrografin diluted in 300 mL of water. The homogeneity of fluid tagginame case the fluid appears homogeneously tagged (even if with a lower density) in

. Fecal and fluid tagging

Even with full-dose bowel cleansing regimens, residual stool canamper interpretation of CT colonography. Therefore, oral taggingf colonic fluid and stool with positive (either iodine or barium)ontrast material has been proposed as an alternative to purgationlone in an attempt to help differentiate polyps from residues [26].his way, stool and fluid residues mix with contrast medium andherefore have increased density compared with the normal colonicalls and polyps or tumors, which typically have soft tissue den-

ity. Regardless of the specific tagging method used, any taggingcheme should ideally increase the density of stool and fluid to aalue between 200 and 800 Hounsfield Units (HU) (Fig. 2).

Contrast medium is administered orally at every meal, typicallyhe day before CTC. As the mixture between food and contrastasses through the bowel, nutrients are digested and absorbed,hile the tagging agent becomes more concentrated within thendigested residue and colonic fluid.

Fecal and fluid tagging has several advantages over untaggedreparation techniques. First, diagnostic accuracy is improved dueo easier and more accurate differentiation of “submerged” polypsrom fecal residue. Second, oral tagging allows to use less aggressiveegimens and cleansing protocols, thus increasing patient com-liance. Indeed, a relatively large amount of tagged fecal residue

n the large bowel can be tolerated by the reader without com-

romising the interpretation of CT colonography findings, becauseagged fecal residues can be easily distinguished from true lesions.n this latter perspective, a laxative-free fecal tagging approach toTC has been evaluated, yielding 100% per-patient and per-lesion

lmost equal between ascending, transverse and descending colon (a and b). In theigmoid colon and in the rectum (c and d).

sensitivity for colonic polyps larger than 10 mm [27]. Althoughlaxative-free CT colonography has not yet been extensively val-idated, it has a great potential for dramatically reducing patientdiscomfort and thereby increasing patient acceptance.

Fecal tagging can be performed using barium, iodine, or a com-bination of both.

10. Solid stool tagging with oral administration of barium

Lefere et al. are the first authors who assessed the feasibilityof fecal tagging (FT). In a study with a cohort of 50 patients, thecontrol group received a standard PEG-based preparation, while inthe experimental group bowel preparation included a low-residuediet, mild bowel cleansing with magnesium citrate and bisacodyl,and oral administration of a barium suspension the day beforeCT colonography (Fig. 3). FT resulted in more fecal residue thanthe untagged, PEG-based protocol, but improved differentiationbetween fecal residue and colonic polyps (FT specificity, 88%; non-FT, 77%), while sensitivity was comparable (FT, 88%; non-FT, 85%).Moreover, FT led to significantly reduced discomfort, side effects,and sleep disturbances, and resulted in overall higher comfortreported by patients after CT colonography [26].

Barium has proved effective in tagging stool, is well toler-ated and carries virtually no risk of allergic reactions. However,its relatively low water solubility may result in uneven tagging

of residual fluid, which may be problematic in association withreduced cleansing preparation schemes. This latter circumstanceis especially true when electronic cleansing software is intended tobe used in order to remove tagged residues from the colonic lumen,

E. Neri et al. / European Journal of Radiology 82 (2013) 1137– 1143 1141

Table 1Preparation schemes of CT colonography in 6 European diagnostic centers.

Amsterdam Medical CenterDay before examination Low-fiber diet during the whole day

Lunch: 1 × 50 mL Gastro-TelebrixDiner: 1 × 50 mL Gastro-Telebrix

Day of examination (CTC preferably planned in the morning) No solid food before examination, only fluids allowed ≥1.5 h before examination:1 × 50 mL Gastro-Telebrix

University College of London, UKTwo days before examination Low-fiber diet during the whole dayDay before examination 7.30–09.00 am: 1 sachet of Picolax in a cup of cold tap water (approx. 150 mL)

15.00–15.30 pm: as above, 1 sachet of PicolaxDay of examination (CTC preferably planned in the morning) 2 h before examination: oral assumption of Gastrografin (Diatrizoate meglumine) or 30 mL

of Omnipaque 300 (iohexol)

Courtesy of Prof. Stuart TaylorUniversity of Pisa, IT (option 1), Institute for Cancer Research and Treatment, Candiolo, and University of Rome “La Sapienza”, Italy1–3 days before examination Low-fiber diet during the whole day

After breakfast, lunch and dinner 1 sachet of Movicol (13.125 gL) in a glace of waterDay of examination (CTC preferably planned in the morning) 3 h before examination: oral assumption of Gastrografin

University of Pisa, IT (option 2) iso-osmolar reduced-cathartic approach2 days before examination Low-fiber diet during the whole dayDay before examination 16.00: clear liquid diet and 4 × 5 mg bisacodyl (Lovoldyl)

18.00: 4 sachets of LOVOL-ESSE (macrogol) in 2 L of waterDay of examination • 3 h before examination: oral assumption of Gastrografin (100 mL in 300 mL of water)• (CTC preferably planned in the morning) • 3 h before examination: oral assumption of Visipaque 300 (100 mL in 300 mL of water)• 3 tagging schemes • Rectal enema immediately before insufflation (150 mL of Visipaque 270 in 150 mL of

water)

Roselaare Hospital (option 1), BelgiumDay before examination

• 8.00 am: clear liquid diet• Noon: clear liquid diet and 2 × 5 mg bisacodyl (Dulcolax)• 3.00 pm: 1 sachet of Citra Fleet or Picolax, to dissolve in one glass of water (250 mL)• 6.00 pm: clear liquid diet and 225 mL Barium 4.2% w/v• 7.00 pm: 1 sachet of Citra Fleet or Picolax, to dissolve in one glass of water (250 mL)• 9.00 pm: Gastrografin 50 mlRecommendation: drink a glass of water every hour between 3 and 9 pm and avoid drinking after 9 pm

Day of examination No prescriptions

Roeselare Hospital (option 2)Day before examination

• 8.00 am: clear liquid diet and 225 mL of Barium 4.2% w/v• Noon: clear liquid diet, 225 mL of barium 4.2% w/v, and 2 × 5 mg bisacodyl (Dulcolax)• 5.00 pm: clear liquid diet• 6.00 pm: fleet Phosphosoda 45 mL (or Magnesium Citrate, if available)• 9.00 pm: Gastrografin 50 mLRecommendation: drink a glass of water every hour between 3 and 9 pm and avoid drinking after 9 pm

Day of examination No prescriptions

Note: (Commercial names of cathartic and tagging agents, and corresponding farmaceutical preparation): Dulcolax: bisacodyl (5 mg × 1 capsule). Fleet phospho-soda: sodiump n: sodb rogol

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hosphate monobasic 21.6 g, and sodium phosphate dibasic 8.1 g (45 mL). Gastrografiisacodyl (5 mg × 1 capsule). Lovol-ESSE: macrogol (64.5 g × 1 sachet). Movicol: macagnesium oxide 3.5 g, citric acid 12 g. Telebrix: ioxithalamate.

s such algorithms require optimal tagging homogeneity to workest.

1. Fluid tagging with oral administration of iodinatedontrast medium

Oral administration of hyperosmolar iodinated CM providesomogeneous tagging of both fluid and solid residues and sti-ulates fluid secretion into the colon, thus creating a smooth

iquid-to-air interface that improves the performance of digitalubtraction software.

Iannaccone et al. showed that the addition of diatrizoateodium and diatrizoate dimeglumine (Gastrografin) to regulareals (180 mL × 6 meals) led to a sensitivity as high as 95.5% for

he identification of colorectal polyps sized equal to or greater than mm. In this study no cathartic agents were administered, as Gas-rografin acted both as a fecal tagging and bowel cleansing agentwing to its hyperosmolarity [27].

ium amidotrizoate 100 mg/mL and meglumine amidotrizoate 660 mg/mL. Lovoldyl:(13.8 g × 1 sachet). Omnipaque: iohexol 300 mg. Picolax: sodium picosulfate 10 mg,

However, iodinated contrast medium (and especially ionicones, such as Gastrografin) may cause side effects ranging frommild symptoms (such as diarrhea, nausea, or vomiting) to evenlife-threatening (although rare) allergic reactions, so that theiradministration outside hospitals is not recommended. Moreover,a small amount of iodinated contrast is absorbed by the colonicmucosa and can be detected in the bloodstream, even if adminis-tered orally or introduced into body cavities. Such resorption maycause hypereosinophilia, which may predispose the patient to thedevelopment of allergic reactions. Finally, ionic iodinated contrastmedium such as Gastrografin draw fluids inside the colon due totheir hyperosmolarity, thus carrying the risk of electrolyte imbal-ance.

For the above reasons, Neri et al. conceived the same-day prepa-ration technique, consisting of a low-residue diet and reduced

cathartic preparation with a mild laxative (PEG macrogol 3350) ateach of the three main meals, starting two days before CTC. On theday of CTC, patients drink a 50 mL solution of sodium diatrizoateand meglumine diatrizoate (total iodine load 18.5 g) diluted in

1142 E. Neri et al. / European Journal of Ra

Fig. 5. (a) Preparation regimen with PEG as cleansing agent and fluid tagging withrectal enema of water-iodine solution. (b) A water solution of 150 mL of Visipaque270 in 150 mL of water is rectally introduced just before patient’s insufflation on theCT table. (c) To ensure homogeneous distribution and mixing of contrast it’s askedpatient to turn himself on the CT table. (d) The fluid appears homogeneously taggedin all colonic segments.

diology 82 (2013) 1137– 1143

500 mL of water three hours before CTC, inside hospital and undermedical control. This technique has been shown to provide optimalfluid tagging and is well tolerated (Fig. 4) [28].

In a study by Campanella et al., three different iodine-basedfecal tagging bowel preparation schemes were compared. Consid-ering preparation quality alone, the best technique resulted tobe a 2-day regimen of iodine and phosphosoda administered atmealtime, but the same-day preparation provided the best bal-ance between bowel preparation quality and patient acceptability[29].

12. Tagging with oral administration of barium andiodinated contrast medium

In 2003 Pickhardt et al. proposed the association of barium andiodinated contrast medium for CTC tagging. Patients received astandard 24-h colonic preparation based on oral administration of90 mL of sodium phosphate and 10 mg of bisacodyl. As a part of theirclear-liquid diet, patients also ingested 500 mL of barium for solidstool tagging and 120 mL of Gastrografin for luminal fluid enhance-ment. Sensitivity and specificity of CTC obtained with this regimenwere very high with CTC scoring as well as optical colonoscopy in2 large trials [20].

13. Fluid tagging with rectal enema of water–iodinesolution

This approach is not yet validated in the clinical practice andconsists in a reduce-cathartic preparation the day before the exam,and the introduction of a water solution of iodinated contrastmedium during patient’s insufflation on the CT table. The contrastmedium proposed is Gastrografin or Iodixanol 270. Compared withoral iodine tagging, rectal tagging allowed for significant reduc-tion of examination time with comparable tagging quality andhigh patient acceptance [30] (Fig. 5) (see the detailed preparationscheme in Table 1).

14. Conclusion

To date there is no consensus about the best bowel cleansingpreparation and tagging techniques. Nonetheless, it is important toknow the strengths and weaknesses of each protocol in order tochoose the best approach for optimizing the diagnostic quality ofCT colonography in each patient.

Conflict of interest

No one of the authors received financial support or had personalconnections that could be perceived to bias their work.

Acknowledgements

The authors acknowledge Andrea Laghi (University of Rome“La Sapienza”, Italy), Daniele Regge (Institute for Cancer Researchand Treatment, Candiolo, Italy), Jaap Stoker (Department of Radiol-ogy, University of Amsterdam, The Netherlands), and Stuart Taylor(Department of Diagnostic Imaging, University College of London,UK), for providing the CT colonography preparation schemes usedin their local practice (listed in Table 1).

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