Keywords
computed tomography enterography - gut transit time - oral contrast ingestion time
- polyethylene glycol
Introduction
Despite advances in technology, the mesenteric small bowel continues to elude the
reach of the endoscope. The barium meal follow through (BMFT) and the small bowel
enteroclysis were the most commonly performed radiological examinations in suspected
small bowel pathology.[1]
[2] Recently, computed tomography (CT) and magnetic resonance imaging (MRI) of the abdomen
after distension of the small bowel with neutral oral contrast, termed CT enterography
(CTE) and MR enterography, have been increasingly advocated as an alternative to barium
studies in view of the cross-sectional display of extraluminal structures, greater
patient tolerance, and reduced procedural risks.[3]
[4] The CTE with large volume oral contrast agent administered over a specified period
of time provides adequate luminal distension and separation of small bowel loops,
enabling high diagnostic accuracy for small bowel pathology. In CTE, detailed evaluation
of the entire length of the small bowel is possible because of the uniform distension
achieved by the ingestion of large volumes of contrast in a relatively short period
of time. Thus, CTE allows simultaneous assessment of the lumen, wall thickness, and
pattern of wall enhancement. CTE also eliminates the pitfalls associated with small
bowel superimposition, allowing excellent depiction of mural and extraintestinal abnormalities.
Multiple oral contrast agents including positive, negative, and neutral contrast agents
have been tried to achieve small bowel distension on CT and it has been concluded
that neutral oral agents are the most suitable for evaluation of small bowel pathology.[5]
[6]
[7]
[8]
[9] In our study, we used polyethylene glycol (PEG) electrolyte solution to distend
small bowel. Currently, the most commonly used CTE protocol is high volume (2 L) oral
neutral contrast such as mannitol or PEG ingested over 1 hour 20 minutes.[3]
[4]
[5] Gut transit time can, however, vary with different populations. Indians have a shorter
gut transit time as compared with Western population. Several factors such as age,
gender, dietary habits, lifestyle, and biological differences may contribute for shorter
gut transit time among Indians[10]
[11]
[12]
[13]
[14]
[15]
[16]
[17] with mean stool frequency being higher in several Asian populations. For example,
a stool frequency of thrice a week (range: 3–21 per week) is considered normal in
a Western population, while Indians have a stool frequency of at least one stool per
day. Two stools per day is considered as normal among Indians.[16]
Timing of contrast ingestion in enterography may therefore not be uniformly applicable
to all populations. Given the rapid gut transit in Indians, we reduced the oral contrast
ingestion time to 45 minutes and compared this with the standard protocol of 1 hour
20 minutes described in the literature. This study is therefore proposed to prospectively
evaluate the luminal distension with shorter contrast ingestion time among Indians
in comparison with the 1 hour 20 minutes ingestion time protocol.
Materials and Methods
Patients and Control Subjects
Our study is a prospective observational study with study population of 42 patients
in the age group of 18 to 75 years referred to radiology for contrast-enhanced CT
of the abdomen and pelvis to evaluate suspected small bowel pathology. All patients
with a clinical suspicion of high grade, acute intestinal obstruction were excluded
from the study. Other exclusion criteria included pregnancy, history of allergy to
iodinated contrast, history of severe drug allergy, renal insufficiency with serum
creatinine > 1.5 mg/dL, and inability to ingest > 1 L of contrast. The patients were
instructed to remain nil orally for solids for at least 4 hours prior to the start
of CTE.
The CTE was performed in 42 consecutive patients divided into two equal groups—A and
B. Group A patients were instructed to drink 2 L of neutral oral contrast (PEG electrolyte
solution) over 1 hour 20 minutes. Group B patients were instructed to do the same
over 45 minutes. At the end of contrast ingestion, routine CT abdomen was performed
and the patient observed for 1 hour before leaving the hospital with an instruction
to return to the hospital in case of serious side effects. Written informed consent
was obtained from all patients. The study was conducted after Institutional Review
Board and Ethics committee approval of the study protocol.
Image Acquisition
All scans were performed on a 64-slice CT scanner (Toshiba Aquilion). Using a pressure
injector, 150 mL of intravenous (IV) Omnipaque (300 mg/mL) was injected 4 to 4.5 mL/second.
Administration of contrast was followed by a flush of 40 mL normal saline at the same
injection rate. A dual-phase CT scan was performed after an unenhanced CT scan. Bolus
tracking method was used for acquisition of arterial and enteric phases; the trigger
was placed on the descending thoracic aorta, arterial phase acquired after a delay
of 15 to 20 seconds, and enteric phase after a delay of 45 seconds postthreshold achievement
in the lower thoracic aorta.
Postprocessing
Images were acquired in the axial plane in a cephalocaudal direction, from the hepatic
dome to the symphysis pubis, during one breath hold. Raw data were generated in axial
planes with 3-mm thickness, later reconstructed in coronal and sagittal planes with
a section thickness of 3 mm and reconstruction interval of 1 to 1.5 mm. Images were
transferred to picture archiving and communication system for review. In addition,
the 0.625-mm raw data were transferred to the workstation for three-dimensional volume
rendering and maximum-intensity-projection displays.
Image Analysis
Manual quantitative analysis of the degree of small bowel distension was performed
in the following manner: on coronal images, the abdominal cavity was divided into
four quadrants: right upper, left upper, right lower, and left lower quadrants. The
maximum small bowel lumen diameter (inner-to-inner wall) was measured in five different
loops within each of the four quadrants. If 4 or more measurements in a quadrant ≥
1.8 cm (considered “adequate luminal distension”), a score of 1 was assigned to that
quadrant. If less than 4 measurements in the quadrant > 1.8 cm, a score of 0 was assigned
to that quadrant. The ensuing sum of scores from all four quadrants resulted in the
distension grade for that CTE study (Grades 1–4).
If each of the four quadrants scored 1, then distension grade for that CTE study is
Grade 4. Similarly, if sum of all the four quadrants is 3, then the distension grade
for that CTE study would be Grade 3, if sum of all four quadrants is 2, then the distension
grade would be Grade 2, and if sum of all four quadrants is 1, then the distension
grade would be Grade 1.
|
Sum of all 4 quadrants
|
Distension grade for the CTE study
|
|
4/4
|
Grade 4
|
|
3/3
|
Grade 3
|
|
2/4
|
Grade 2
|
|
1/4
|
Grade 1
|
Grades 4 and 3 were considered to have optimal bowel distension ([Figs. 1]
[2]
[3]
[4]), while Grades 2 and 1 ([Figs. 5]
[6]
[7]
[8]
[9]) were considered to have poor bowel distension. None of our patients had Grade 1
distension.
Fig. 1 Axial (A) and sagittal (B) reconstructed computed tomography (CT) enterography images in enteric phase of a
30-year-old female patient showing Grade 4 distension score.
Fig. 2 A 24-year-old male patient with normal computed tomography (CT) enterography study.
Coronal reformation through abdomen in enteric phase demonstrating Grade 3 distension
score.
Fig. 3 A 73-year-old female patient, proven case of Crohn's disease with Grade 3 distension
score computed tomography (CT) enterography study. Axial (A) and coronal reformation (B) through abdomen in enteric phase demonstrating both poorly distended (short arrows)
loops and well distended (long arrows) small bowel loops. The image also demonstrates
engorged vasa recta (positive comb's sign) (white circle).
Fig. 4 Computed tomography (CT) enterography study (with Grade 4 distension score) of a
36-year-old male patient, known case of Crohn's disease presented with recurrent pain
abdomen 1 year post-resection. Coronal reformation in enteric phase shows short segment
stricture with wall thickening and marked enhancement suggesting recurrence at the
anastomotic site (long arrow). The short arrow points to another similar segment (just
inferior) with wall thickening, enhancement, and pseudosacculations (short arrow).
Fig. 5 A 26-year-old female patient, proven case of abdominal tuberculosis. Axial computed
tomography (CT) enterography image in enteric phase demonstrating Grade 2 distension
score with collapsed small bowel loops. The image shows asymmetrical wall thickening
involving ileocecal junction (arrow) with multiple necrotic mesenteric lymph nodes
in right lower quadrant.
Fig. 6 A 30-year-old female patient, biopsy-proven case of Crohn's disease demonstrating
Grade 2 distension score computed tomography (CT) enterography study. Coronal reformation
through the abdomen in the enteric phase shows skip lesions in the ileal loops located
in the right lower quadrant (arrows).
Fig. 7 Computed tomography (CT) enterography study with Grade 2 distension score in a 35-year-old
male patient, known case of Crohn's disease presented with recurrent pain abdomen.
Axial CT enterography image in enteric phase demonstrating pseudosacculations along
the antimesenteric border of sigmoid colon and shortening of the mesenteric border
(arrow).
Fig. 8 A 37-year-old male patient, biopsy-proven case of Crohn's disease. Axial (A) and sagittal (B) reformatted plain computed tomography (CT) enterography image with Grade 2 bowel
distension. Stratified wall thickening (arrows) is seen in the affected distal ileal
segment.
Fig. 9 Computed tomography (CT) enterography study of a 37-year-old male patient, suspected
case of Crohn's disease demonstrating poor/Grade 2 distension score. Axial (A) and reconstructed coronal (B) CT enterography image in the enteric phase shows thickening of the ileocecal junction,
terminal ileal loop with engorged vasa recta/positive Comb's sign (short arrows).
The image also demonstrates enhancing appendix (long arrows). Histopathological examination
(HPE) revealed Crohn's disease.
Data were tabulated and analyzed using statistical methods.
Statistical Analysis
Descriptive and inferential statistical analyses were done on the data collected and
tabulated. Results on continuous measurements are presented as mean ± standard deviation
(min–max) and results on categorical measurements presented in number (%). Chi-square/Fisher's
exact test was used to find the significance of study parameters on categorical scale
between two or more groups.
Statistical software: The Statistical software, namely SAS 9.2, SPSS 15.0, Stata 10.1,
MedCalc 9.0.1, Systat 12.0, and R environment ver.2.11.1 were used for the analysis
of the data and Microsoft Word and Excel were used to generate graphs, tables, etc.
Results
Both the protocols were well tolerated by the patients, without any discomfort; none
of the 42 patients who ingested 2 L PEG solution reported any major side effects.
Forty-two patients ingested 2 L of oral contrast in the stipulated time without significant
nausea or abdominal discomfort. There was a statistically significant difference in
the degree of small bowel distension between the two groups with better distension
seen in group B with shorter contrast ingestion time protocol (p < 0.001). Grade 4 distension was achieved in only 9.5% of group A subjects with the
longer 1 hour 20-minute protocol as against 42.9% in group B. Grade 3 distension was
achieved only in 33.3% of group A subjects as against 42.9% of group B. Overall, adequate
and more uniform distension of small bowel was achieved with the group B 45-minute
ingestion protocol compared with the group A 1 hour 20-minute protocol ([Table 1], [Fig. 10]).
Table 1
Comparison of small bowel diameter in two groups with different contrast ingestion
times: Group A (1 hour 20 minutes) and group B (45 minutes)
|
Group A
|
Group B
|
p-Value
|
|
*Statistically significant (p < 0.05).
|
|
Right upper quadrant
|
1.92 ± 0.26
|
2.14 ± 0.28
|
0.013*
|
|
Left upper quadrant
|
2.76 ±3.74
|
2.25 ±0.31
|
0.541
|
|
Right lower quadrant
|
2.04 ±0.33
|
2.20 ±0.34
|
0.112
|
|
Left lower quadrant
|
1.95 ±0.26
|
2.16 ±0.32
|
0.021*
|
Fig. 10 Comparison of small bowel diameter in two groups.
Incidence of small bowel pathology was analyzed in two groups separately. 47.6% patients
of group A had small bowel pathology while 23.8% of patients in group B had small
bowel pathology. Thus, the bias associated with small bowel pathology induced shorter
transit times was eliminated ([Tables 1]
[2], [Figs. 1]
[2]
[3]
[4]
[5]
[6]
[7]
[8]
[9]
[10]
[11]).
Table 2
Grade/Distension scores
|
Grade/distension score
|
Group A (number)
|
Group A Percentage (%)
|
Group B (number)
|
Group B Percentage (%)
|
|
Grade 1
|
0
|
0.0
|
0
|
0.0
|
|
Grade 2
|
12
|
57.1
|
3
|
14.3
|
|
Grade 3
|
7
|
33.3
|
9
|
42.9
|
|
Grade 4
|
2
|
9.5
|
9
|
42.9
|
|
Total
|
21
|
100
|
21
|
100
|
Fig. 11 Grade/distension score—comparison between two groups: Group I (A) and group II (B).
Discussion
Computed Tomography Enterography
Despite advances in technology, the mesenteric small bowel continues to elude the
reach of the endoscope and provides the biggest challenge in bowel imaging. This is
mainly due to the length, redundancy, overlap, and small caliber of the small bowel.
Because of the overlapping nature of bowel loops in the pelvis, inadequate and nonuniform
distension of loops, lengthy procedure time, barium-related complications, and operator
dependence associated with barium studies, cross-sectional imaging studies are becoming
more popular for evaluation of small bowel pathology. Cross-sectional imaging of small
bowel includes CT and MRI with oral and IV contrast agents. These studies not only
prevent obscuration of small bowel loops by superimposition, but also depict mural
and extraintestinal complications of the disease. They provide better depiction of
small sinus tracts, abscesses, fistulas, and ulcerations especially when combined
with oral contrast agents either via enterography or enteroclysis.[1]
[2]
The CT abdomen after distension of the small bowel with neutral oral contrast, termed
CTE, has been increasingly advocated as an alternative to barium studies. CTE is a
simple, noninvasive radiological investigation for evaluating small bowel and can
be used as the primary investigation in suspected small bowel pathology. Irrespective
of the CT technique used, adequate bowel distension is mandatory since mural thickening
is the hallmark of small bowel disease. Complete evaluation of the small bowel is
achieved with the addition of IV contrast and a large volume of neutral contrast to
distend the intestinal lumen, allowing assessment of the lumen, thickness, and pattern
of enhancement of the small intestinal wall. The CTE with large volume of neutral
oral contrast agent provides adequate luminal distension and separation of small bowel
loops, thus accounting for a high diagnostic accuracy for small bowel pathology. Currently,
CTE is commonly performed using high-volume (2 L) oral neutral contrast agents such
as mannitol or PEG ingested over 60 to 90 minutes followed by an IV contrast. Many
authors have reported CTE to be highly sensitive and specific in the diagnosis and
characterization of various small bowel pathologies. Solem et al performed a comparison
study between CTE, ileocolonoscopy, capsule endoscopy, and BMFT on 41 patients with
Crohn's disease and concluded that the sensitivity of CTE was equal to that of capsule
endoscopy (83%) and more than that of ileocolonoscopy (74%) and BMFT (65%). In this
study, specificity of CTE (82%) was found to be less than that of ileocolonoscopy
(100%) but more than that of capsule endoscopy (53%) and BMFT (94%).[18] In 2011, Minordi et al compared CTE and CT enteroclysis in 145 patients. Seventy
patients underwent CT enteroclysis after jejunal intubation and infusion of methylcellulose,
and 75 patients underwent CTE after orally ingesting 2 L of PEG solution over 45 minutes.
CTE showed findings of Crohn's disease as well as CT enteroclysis, although CT enteroclysis
gave better bowel distension, especially in the jejunum, and had a higher specificity
than CTE.[19]
A study performed in 2011 by Huprich et al on 22 patients demonstrated that multiphasic
CTE was more than twice as sensitive as capsule endoscopy for finding the source of
obscure gastrointestinal (GI) bleeding (88 vs. 38%).[20] In India, Sodhi et al in 2012 performed CTE on 35 patients with occult GI bleed—15
had positive findings that were confirmed on exploratory laparotomy. They concluded
that CTE was a useful investigation tool in the evaluation of both occult and overt
GI bleeding.[21]
Polyethylene Glycol as Oral Neutral Contrast Agent
Multiple oral contrast agents have tried to achieve small bowel distension on CT including
positive, negative, and neutral contrast agents. Neutral oral agents have been found
to be the most suitable for the evaluation of small bowel pathology.[5]
[6]
[7] PEG electrolyte solution has been shown to distend small bowel better than water
or methyl cellulose solution as well as low-density barium.[8]
[9] The neutral oral contrast agent in conjunction with IV contrast results in the depiction
of the lumen as well as the thickness and enhancement pattern of the wall. PEG electrolyte
solution is the best known neutral contrast used widely as a colonoscopy preparatory
agent. It is easily available, less expensive, palatable, and has no known serious
side effects.[5]
[6]
[7]
[8]
[9] CTE with PEG solution was performed by Minordi et al and found to be 93% sensitive
and 94% specific compared with CT enteroclysis that had a sensitivity of 94% and specificity
of 100%.[19] In our study, PEG electrolyte was well tolerated in concordance with the studies
conducted by Solem et al and Minordi et al.[18]
[19]
Oral Contrast Ingestion Time in Computed Tomography Enterography
It is a well-known fact that gut transit time varies widely with different populations,
races, and ethnicity. Age, gender, dietary habits, degree of physical activity, and
biological factors are some factors influencing the gut transit time. Hence, GI protocols
used in one population may not be globally applied on all populations.[10]
[11]
[12]
[13]
[14]
[15]
[16]
[17] There is paucity of literature on normal range of gut transit time in healthy Indian
subjects and ideal or standard oral contrast ingestion time to be used among Indian
population. However, Indians are found to have a rapid gut transit time compared with
the Western population. The stool frequency is considerably higher among the Asian
population. Mean stool frequency is higher in several Asian populations. For example,
a stool frequency of thrice a week (range: 3–21 per week) is considered normal in
a Western population while Indians have a stool frequency of at least one stool per
day. Two stools per day is considered as normal among Indians.[16] The most commonly used CTE protocol in the West is high-volume (2 L) oral neutral
contrast agents such as mannitol or PEG ingested over 1 hour 20 minutes. In view of
faster gut transit time, we postulated that Indian populations may need a shorter
contrast ingestion time. In our study, we decreased the oral contrast ingestion time
to 45 minutes and compared this with the standard protocol of 1 hour 20 minutes described
in the literature. We found that ingestion of oral contrast over a period of 1 hour
20 minutes provided suboptimal distension of the small bowel, particularly the jejunum
with more uniform distension of the colon. This is likely due to rapid gut transit
time among Indians. Administration of the oral contrast agent over a period of 45
minutes resulted in improved distension of the jejunum and a more uniform distension
of the small bowel. A similar protocol of a 45-minute oral contrast ingestion time
was recommended for optimal bowel distension by Ilangovan et al[4], where patients were instructed to drink 2 L of 2.5% mannitol solution over 45 minutes.
Minordi et al in 2011also used a similar protocol with 2 L of PEG solution administered
over 45 minutes and achieved optimal bowel distension. Their study concluded that
results obtained with PEG CTE using the 45-minute oral contrast ingestion protocol
for demonstrating findings of Crohn's disease was comparable with that of CT enteroclysis.[19]
Limitations: We addressed bias due to shortening of gut transit because of small bowel
disease, by comparing the occurrence of small bowel pathology between the two groups.
We found that the shorter ingestion protocol group had fewer patients with small bowel
pathology (24 vs. 48%), thus eliminating this potential bias. However, our study had
other limitations: our sample size of 42 was relatively small and we did not match
our patients for age, gender, or diet in the two groups; intrinsic differences in
gut transit time between the two groups were therefore not corrected.
Conclusion
Gut transit time can vary amongst different ethnicities. CTE contrast ingestion protocols
need to be optimized for specific populations. Populations with faster gut transit
time need shorter oral contrast ingestion time. CTE contrast ingestion protocols optimized
in one population may not be suitable in another population. We found statistically
significant improvement in small bowel distension with the shorter 45-minute ingestion
CTE protocol compared with the 1 hour 20-minute protocol recommended by many authors.
Ours is the first study to compare two contrast ingestion time protocols in an Indian
population. To the best of our knowledge, there are no other studies comparing CTE
oral contrast ingestion time protocols in a given population. Further studies with
a larger sample size are recommended to investigate optimum oral contrast ingestion
protocols for CTE among different populations.
