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Pictorial Essay Australasian Radiology (2006) 50, 289–297

Small bowel CT-enteroclysis: Technique, pitfalls and


pictorial review
FJ Parrish
Symbion Health, Noosa Hospital and Specialist Centre, Noosaville, Queensland, Australia

SUMMARY
Computed tomography small bowel enteroclysis has been carried out at Noosa Hospital since July 2003, and more
recently at St George Private Hospital, Kogarah. Over 125 cases have been carried out. This article describes the dif-
ferent techniques, the pitfalls and a pictorial review of small bowel pathology.

Key words: computed tomography; pictorial review; pitfall; small bowel enteroclysis; technique.

INTRODUCTION TECHNIQUE
The established method of imaging of the small bowel for non- Indications
acute indications has been by barium examinations. The The main indications for small bowel imaging are periumbilical
debate has continued for many years regarding which examin- pain, unexplained iron deficiency anaemia, weight loss, diar-
ation should be carried out, among either the small bowel rhoea or recurrent small bowel obstruction.
enema or barium follow-through.
Small bowel pathology is relatively rare when compared with Contraindications
that in the upper and lower gastrointestinal tract.1 These are few, with gross perforation or acute complete ob-
In recent years, there has been renewed interest in small struction being the only absolutes. Allergies or contraindications
bowel imaging using a variety of techniques, such as CT, MRI, to iodinated contrast media and buscopan are relative and can
CT and MRI enteroclysis and the small bowel capsule. Computed be overcome by modifying the technique.
tomography-enteroclysis (CT-E) has been carried out since the
mid-1990s, but early results were indifferent because of the poor Preparation
volume imaging of single-slice CT.2 More recently, there has been This is required before the use of i.v. contrast and to clean the
renewed interest with the advent of multi-slice CT technology. No bowel. The colon should be clean, as faecal loading in the cae-
single source of information is available in the literature, giving an cum can retard the flow of contrast into the ileum.3 Faeces can
overview of the different techniques and the pitfalls for radiologists also be present in the distal ileum. Typically, an 8-h fast and
wishing to provide this imaging technique. mild laxatives are required.
Since July 2003, CT small bowel enteroclysis has been The technique is not pleasant and it is useful to have an
undertaken at Noosa Hospital and more recently at St George information sheet to give patients before the examination. This
Private Hospital, Kogarah, New South Wales. Over 125 cases helps explain the preparation, procedure and post procedure
have been carried out. All of them were referred by specialist events.
surgeons and gastroenterologists.
The aim of this article is to describe the different techniques Contrast
of CT-E, the pitfalls seen and to provide a pictorial review of There are different techniques that can be used: negative
small bowel pathology observed. (Fig. 1), low (Fig. 2) or high (Figs 3,4) small bowel contrast.

FJ Parrish, FRCR, FRANZCR.


Correspondence: Dr FJ Parrish, Radiology, Level 2, St George Private Hospital, South Street, Kogarah, NSW 2217, Australia.
Email: frank.parrish@gmail.com
Submitted 19 August 2004; accepted 1 February 2006.
doi: 10.1111/j.1440-1673.2006.01587.x

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Journal compilation ª 2006 Royal Australian and New Zealand College of Radiologists
290 FJ PARRISH

Fig. 3. High bowel contrast. The large soft tissue mass encasing small
Fig. 1. Negative bowel contrast. This variation provides the best delin- bowel is lymphoma.
eation of the small bowel wall. Note the abnormal bowel wall and mes-
enteric inflammatory change due to Crohn disease.
enabling the density to be easily adjusted. Methyl cellulose
has been traditionally used to ensure adequate distension.
Each of these techniques can be used with or without i.v. con-
Recently, it has been shown that a negative contrast examin-
trast. There is no evidence in the literature to support any one
ation with good distension can be achieved by using water
of these techniques over the others.
alone.4
Table 1 describes the different small bowel contrast mix-
The mixture density can be easily modified to take into
tures. Iodinated contrast is used in addition to the barium,
account different equipment and personal preferences.

Fig. 2. Low bowel contrast. This shows the different contrast densities
that can be achieved. Extra iodinated contrast was added to the first Fig. 4. Volume rendered high bowel contrast. High contrast allows
syringe. This was injected with the tube at the pylorus for a better view to volume rendered images, which show the multiple small bowel loops
enable passage of tube into the duodenum. involved in the small bowel lymphoma of Figure 3.

ª 2006 The Author


Journal compilation ª 2006 Royal Australian and New Zealand College of Radiologists
SMALL BOWEL CT ENTEROCLYSIS 291

Table 1. Ingredients procedure and aspiration can occur in the sedated patient. For
this reason, sedation has not been given at Noosa.
Contrast density Negative Low High
A nasoenteric tube, such as a Bilboa–Dotter tube (Cook),
Methyl cellulose (mL) 40 40 40
is then passed under screening into the distal duodenum around
Boiling water (mL) 400 400 400
the duodenal–jejunal (D–J) flexure. The technique of duodenal
CT barium (scan C or E-Z-Cat) (g) — 5 —
Screening barium (g) — — 125 intubation has been well documented in the literature.5 The
Iodinated contrast 300 mg/mL — 40 — Bilboa–Dotter tube comes complete with a technique booklet. If
Bubble breaker (mL) 20 20 20 the tube is not placed around to the D–J flexure, regurgitation into
Cold water (mL) 2500 2500 2500 the stomach and subsequent vomiting can occur.
Once the tube is in place, the mixture is injected at approxi-
The procedure typically requires approximately 2 L of mix-
mately 120 mL/min. Care needs to be taken to ensure that no
ture, but not uncommonly more. Although smaller amounts can
bubbles are injected with the mixture. A pump is the ideal
be made, if methyl cellulose is used, it is difficult to make quickly
method for administration; however, pumps are expensive
if more is required. Furthermore, disruption of the ensuing con-
and using a radiographer/nurse is a cheaper alternative.
trast column can occur.
Intermittent screening is carried out until the mixture is seen
Preparing the mixture is of critical importance, as there is
in the descending colon. Stopping before this point usually
a propensity for the mixture to coagulate into lumps. The use of
results in poor distension of the terminal ileum. It is also useful
premium grade methyl cellulose is recommended for this rea-
to have the caecum distended, allowing a good view of the
son. Table 2 describes the recipe for preparing the mixture.
terminal ileum and, where present, the appendix.
Negative contrast gives a good view and may allow obser-
Buscopan (Boehringer Ingelheim, North Ryde, Australia)
vational enhancement of the bowel wall. It cannot be followed
20–40 mg i.v. is given at this time and the tube is removed.
by screening and hence relies on the patient reporting the need
The patient is then immediately transferred to the CT scanner.
to defecate, to ensure transit.
High-contrast examinations allow information to be gath- CT
ered during screening. The resultant CT, however, is degraded The CT protocols used are dependent on the type of machine,
and visualization of the wall is poor. In addition, there is an but basically require high-resolution imaging with a slice width
increase in the dose required to penetrate the contrast. of approximately 1 mm. The whole abdomen should be
Most of the examinations that were carried out at Noosa scanned in a single breath-hold. This ensures that high-quality
used the low-contrast technique. Positive bowel contrast shows multi-planar reformats can be produced. Coronal images are
luminal lesions better than negative contrast and, in the author’s the best planes for displaying the examination. Workstation
opinion, are easier to review. review is extremely helpful to allow reconstruction along the
long axis of the small bowel in areas of concern.
Procedure
The intubation and infusion are best carried out in a screening Radiation dose
room followed by transfer to CT, once the mixture has passed The radiation dose given depends on many factors, including
into the proximal descending colon. the type of CT, the screening unit and the contrast density used.
Nasal topical anaesthetic is applied using a lignocaine spray The low-contrast technique gives a dose similar to that of a
while the patient sniffs up. This allows for some anaesthetic to standard CT abdomen with oral contrast. In addition, there is,
reach the nasopharynx. It is useful to spray liberally around the on average, 4 min of low-dose screening time.
superior aspect of the nasal orifice as this is the area where
patients find the tube causing most discomfort. Complications
Once this has been carried out it is the ideal time to secure Major complications are rare, but include tube trauma, aspir-
i.v. access (and allow the lignocaine to work). Some radiologists ation and reactions to the pharmaceuticals used.
give i.v. sedation at this point. There is a risk of vomiting with the Minor complications relate to the pharmaceuticals utilised
and diarrhoea.

Table 2. Recipe PITFALLS


1 Failure of cannulation. With the use of screening and practice
Mix methyl cellulose with boiling water
Add bubble breaker – stir this is a rarity.
Add iodinated contrast – stir 2 Inadequate preparation. Faecal residue can delay the pas-
Add barium – stir sage of contrast into the terminal ileum. Usually residue is
Add cold water – stir recognizable by its angular shape, but excluding small lesions
Add ice if mixture is too warm
in the presence of faeces is difficult (Fig. 5).

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Journal compilation ª 2006 Royal Australian and New Zealand College of Radiologists
292 FJ PARRISH

Fig. 5. Poor preparation. Angular filling defects are present in the dis- Fig. 7. Delay before CT. Good distension of the distal small bowel and
tal ileum consistent with faeces. caecum, but the proximal bowel (arrow) has collapsed.

3 Injecting too fast. If the contrast is injected too fast, reflux 5 Cease before reaching the colon. By screening and ceasing
and subsequent vomiting can occur. Pulmonary aspiration is only when contrast reaches the descending colon, this can be
a possibility with the nasojejunal tube in place and avoided. This is more of a problem if a negative contrast tech-
local pharyngeal anaesthetic. Vomiting also breaks up the col- nique is used.
umn of contrast and reduces the bowel distension 6 Breathing artefact during CT. Axial imaging should still allow
(Fig. 6). the diagnosis to be made in most cases. Subtle abnormalities
4 Delay between removing the tube and CT. The column of may be missed.
contrast moves on, so that good views of the caecum are 7 Too much gas. Makes interpretation difficult and requires
obtained but the upper jejunum collapses (Fig. 7). constant workstation windowing (Fig. 8).

Fig. 8. Excess gas. The small bowel is distended with gas rather than
Fig. 6. Injecting too fast with vomiting. The small bowel has collapsed. contrast.

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Journal compilation ª 2006 Royal Australian and New Zealand College of Radiologists
SMALL BOWEL CT ENTEROCLYSIS 293

Fig. 9. Crohn disease distal ileum. The terminal ileum (arrow) is thick
walled when compared with the proximal bowel above. Note again the
difference in bowel wall delineation between high and low contrasts.

Fig. 11. Active Crohn disease with a stricture. The small bowel wall
(open arrow) is thickened with increased density in the surrounding
PICTORIAL REVIEW
mesenteric fat, compatible with inflammatory change. Proximal to the
Crohn disease stricture the bowel wall is still abnormally thick, but the lumen is not
Crohn disease is characterized pathologically by transmural narrowed (closed arrow).
inflammation, non-caseating granulomata, dilatation or sclerosis
of lymphatic channels and lymphoid aggregates.6 There is and the adjacent inflammatory change in the mesentery
a range of disease, from mild inflammatory change to strictures, (Figs 1,11). The technique is useful to delineate not only the
fistulas and abscess formation. Skip lesions are typical. stricture, but also the length of bowel involved on either side
Computed tomography-enteroclysis can show mild wall and the presence of any extraluminal disease. This allows the
thickening (Figs 9,10) through to stricture formation (Figs 11,12)

Fig. 12. Crohn stricture. There is wall thickening (closed arrow) and
Fig. 10. Crohn disease terminal ileum. Wall thickening, with the stricture formation. The normal bowel is dilated proximal to the stricture
barium equivalent of ‘rose thorn’ ulceration. (open arrow).

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Journal compilation ª 2006 Royal Australian and New Zealand College of Radiologists
294 FJ PARRISH

surgeon to plan how much of the bowel may need to be


resected.

Small bowel malignancies


Primary malignancies of the small bowel are rare, with an inci-
dence of 1:100 000.1 They include benign tumours such as
leiomyoma, adenoma and lipoma and malignant tumours,
including carcinoid, adenocarcinoma and lymphoma (Figs 3, 4).
The rare gastrointestinal stromal tumours range from benign to
malignant. Metastases, for example, of the ovary and melanoma,
can occur, which typically arise on the anti-mesenteric border.
Carcinoid tumours are usually found in the terminal ileum
(Fig. 13) and the appendix. They can present as areas of wall
thickening as shown or as a stellate mass due to a desmoplastic
reaction.
Lipomata (Fig. 14) are typically round intraluminal lesions
with a short pedicle. They have an attenuation similar to that
of mesenteric fat.
Fig. 14. Lipoma. The lipoma shown is a round intraluminal lesion with
a similar attenuation to the mesenteric fat.
Small bowel diverticula
These include Meckel’s diverticulum, duodenal diverticulum
and rarer jejunal diverticulosis. A Meckel’s diverticulum (Fig. 17) is a persistence of the
Duodenal diverticula can cause obstruction because of the omphalomesenteric duct. It typically occurs in 2% of the
anatomical location (Fig. 15). population, 2 feet from the ileocaecal valve and measures
Jejunal diverticulosis (Fig. 16) is characterized by bacterial 2 inches. It can contain heterotopic gastric mucosa in 30%.
overgrowth, pain and anaemia. The lymphadenopathy shown Most symptomatic cases present before 10 years of age.
was reactive secondary to bacterial overgrowth and subse-
quent inflammatory change.

Fig. 15. Duodenal diverticulum. A large diverticulum is present just as


Fig. 13. Carcinoid tumour. There is ‘apple core’ type circumferential the duodenum pass between the mesenteric artery and aorta. This was
wall thickening over a short segment. causing intermittent obstruction.

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Journal compilation ª 2006 Royal Australian and New Zealand College of Radiologists
SMALL BOWEL CT ENTEROCLYSIS 295

Fig. 16. Jejunal diverticulosis and reactive lymphadenopathy. The Fig. 18. Intussusception. The classical ‘bull’s eye’ short axis pattern of
jejunal diverticulum (solid arrow) arises from the inferior surface of the intussusception.
jejunum. The lymphadenopathy (open arrow) was reactive.

One patient (Fig. 19) subsequently went to theatre and had no


Intussusception wall lesion shown at laparotomy.
Intussusception in adults was always thought to have a mechan-
ical lead point, but short segment intussusception can occur Other pathology
without a physical mass lesion (Figs 18,19).7 An intussuscep- The use of CT small bowel enteroclysis can help the surgeon
tion length of less than 35 mm is thought to be self-limiting with plan a bypass of abnormal bowel such as in long-standing radi-
a physical wall lesion being unlikely. Both of these cases dem- ation enteritis, causing multiple episodes of small bowel
onstrated had more than one short segment of intussusception. obstruction (Fig. 20).

Fig. 17. Meckel’s diverticulum. Fig. 19. Intussusception. Intussusception in long axis view.

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Journal compilation ª 2006 Royal Australian and New Zealand College of Radiologists
296 FJ PARRISH

DISCUSSION
Computed tomography small bowel enteroclysis is a now an
evolving technique, which has been shown to be sensitive in
the diagnosis of Crohn disease8,9 and small bowel tumours.10
Boudiaf et al. have recently shown a sensitivity of 100% and
a specificity of 95% in the detection of small bowel disease.4
With the advent of new CT scanners the technique has
improved because of improved resolution and faster acquisition
times, enabling high-quality multi-planar reformats. Computed
tomography-enteroclysis has the advantage over conventional
small bowel enteroclysis by being able to image the bowel wall
and extraluminal disease. Fine mucosal detail is obscured,
unless a high contrast and formal enteroclysis is carried out
before the CT component.
Computed tomography-enteroclysis enables significant dis-
tension of the small bowel and should, in theory, show the same
advantages over conventional CT as described in the true yield
of the small-intestinal barium study by Nolan.11 In one study,
CT-E has been shown to have a sensitivity of 88% compared
Fig. 20. Radiation enteritis. Multiple loops of thick-walled distended
with 80% for conventional CT.12
small bowel.
In recent years, other techniques have been developed to
attempt improved diagnostic evaluation of the small bowel.
Other causes for patient‘s symptoms can be eloquently Magnetic resonance imaging small bowel enteroclysis
shown, although they would have been as easily detected by (MRI-E) is a technique similar to that of CT-E. Recent studies
other investigations. A partially obstructing umbilical hernia by Ochsenkuhn et al.13 and Gourtsoyiannis et al.14 have shown
(Fig. 21) is an example. the superiority of MRI-E over conventional enteroclysis in diag-
nosing active small bowel Crohn disease in the small bowel.
Magnetic resonance imaging small bowel enteroclysis has the
advantage of not using ionizing radiation, except for tube inser-
tion. Computed tomography has higher spatial resolution but
lower tissue contrast when compared with MRI and a combin-
ation of study design and the spatial resolution probably
accounts for the findings of Schmidt et al.15 They found better
sensitivity and interobserver error for CT-E when compared
with MR-E in their prospective study.
Wireless capsule endoscopy (WCE) for the investigation
of small bowel disease has dominated the literature over the
last few years. The procedure involves swallowing a capsule-
that transmits images to a receiver on the skin surface. The
capsule is passed through the alimentary tract, imaging at
two frames per second with the data of up to 8 h of images
reviewed. It does not see all of the bowel mucosa or extra-
luminal disease.
Numerous studies have shown greater sensitivity over
conventional enteroclysis and CT-E for the diagnosis of obscure
gastrointestinal bleeding and inflammatory bowel disease
Many of the early studies compared WCE to single-slice
CT; however, a recent study by Voderholzer et al. confirmed
Fig. 21. Periumbilical hernias. One hernia (solid arrow) contains fat
that the WCE has increased sensitivity over high-quality multi-
only the other (open arrow) has a minimally distended loop of small
bowel with a narrow neck to the hernia. This was causing mild intermit- slice CT-E in assessing active Crohn disease.16 In this study
tent obstruction. CT-E was carried out as the initial investigation to exclude

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Journal compilation ª 2006 Royal Australian and New Zealand College of Radiologists
SMALL BOWEL CT ENTEROCLYSIS 297

stricture formation before WCE. In the presence of strictures or 4. Boudiaf M, Ameer J, Soyer P, Bouhnik Y, Hamiz L, Rymer R. Small
previous bowel surgery, the endoscopic capsule can become bowel diseases: prospective evaluation of multidetector row helical
CT enteroclysis in 107 consecutive patients. Radiology 2004; 233:
stuck, necessitating an operative intervention. A recent study
338–44.
by Rastogi et al. found the additional WCE findings had a pos- 5. Whitehouse GH, Worthington BS. Techniques in Diagnostic
itive influence on the clinical outcome in only a small proportion Imaging, 2nd edn. Blackwell, Oxford, 1990.
of patients.17 In Australia, WCE is approximately three times the 6. Cotran, Kumar, Robbins. Robbins Pathologic Basis of Disease,
cost of CT-E. 4th edn. Saunders, Philadelphia, 1989.
7. Lvoff N, Breiman RS, Coakley FV, Lu Y, Warren RS. Distinguish-
With the renewed interest in small bowel imaging, debate
ing features of self-limiting adult small-bowel intussusception iden-
will no doubt occur between standard CT and CT small bowel
tified at CT. Radiology 2003; 227: 68–72.
enteroclysis, as has been so with small bowel enema and bar- 8. Turetschek K, Schober E, Wunderbaldinger P et al. Findings at
ium follow-through. The picture today is, however, more com- helical CT-enteroclysis in symptomatic patients with Crohn’s: cor-
plex with MRI, MR enteroclysis and WCE joining the equation. relation with endoscopic and surgical findings. J Comput Assist
These new techniques are in the process of evolution and more Tomogr 2002; 26: 488–92.
9. Hassan C, Cerro P, Zullo A, Spina C, Morini S. Computed tomog-
research is required. Because of ethical considerations, con-
raphy enteroclysis in comparison with ileoscopy in Crohn’s dis-
trolled trials between all the different techniques are unlikely to ease. Int J Colorectal Dis 2003; 18: 121–5.
occur. 10. Graffke G, Stroszczynski C, Schlecht I et al. [Diagnosis of tumours
As a consequence of different machines, expertise, avail- of the small intestine with the aid of CT contrast enema. Sellink CT
ability and cost it is likely that there will be regional variations in technique evaluated in 63 patients.] Rontgenpraxis 2002; 54: 214–
19. (In German.)
the method of imaging used. Each technique will have its pro-
11. Nolan DJ. The true yield of the small-intestinal barium study.
ponents and antagonists.
Endoscopy 1997; 29: 447–53.
Computed tomography-enteroclysis is still limited to a 12. Wold PB, Fletcher JG, Johnson CD, Sandborn WJ. Assessment of
few centres, but evidence showing the technique to be an small bowel Crohn disease: non-invasive peroral CT enterography
effective tool for small bowel imaging is becoming available. compared with other imaging methods and endoscopy – feasibility
The current clinical role is probably in those groups where study. Radiology 2003; 229: 275–81.
13. Ochsenkuhn T, Herrmann K, Schoenberg SO, Reiser MF, Goke B,
disease is already known or there is a high index of suspicion
Sackmann M. Crohn disease of the small bowel proximal to
for significant small bowel disease, especially if stricture forma- the terminal ileum: detection by MR-enteroclysis. Scand
tion or extraluminal disease is suspected. J Gastroenterol 2004; 39: 953–60.
14. Gourtsoyiannis N, Papanikolaou N, Grammatikakis J, Papamastor-
akis G, Prassopoulos P, Roussomoustakaki M. Assessment of
ACKNOWLEDGEMENT Crohn’s disease activity in the small bowel with MR and conventional
Dr I Curley, FRCS, FRACS, Noosa Hospital and Specialist enteroclysis: preliminary results. Eur Radiol 2004; 14: 1017–24.
Centre, Noosaville, Queensland, Australia. 15. Schmidt S, Lepori D, Meuwly JY et al. Prospective comparison of
MR enteroclysis with multidetector spiral-CT enteroclysis: interob-
server agreement and sensitivity by means of ‘sign-by-sign’; cor-
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ª 2006 The Author


Journal compilation ª 2006 Royal Australian and New Zealand College of Radiologists

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