Diagnostic imaging plays an important role in evaluating small bowel diseases.1 Gastrointestinal radiographic examinations with contrast agents have been used to detect morphological changes such as mechanical obstruction or an abnormal mucosal interface.2 Ultrasonography provides complementary information about wall thickness, wall layers, motility, and the appearance of adjacent structures.3,4 However, these imaging modalities have limitations such as the superimposition of abdominal structures for radiography or luminal gas artifacts for ultrasonography.3,4 Computed tomography has been used for routine examination of the gastrointestinal tract in humans because all gastrointestinal segments can be imaged without superimposition, which provides detailed in formation about extraintestinal abnormal conditions by use of multidetector CT at a rapid scan speed and high resolution.5–8 Computed tomographic examination of the small intestines requires adequate luminal distention to allow adequate evaluation of mural alterations because collapsed bowels can mask pathological wall thickening that may be related to inflammatory or neoplastic conditions.5–12 Pseudothickening of the wall of collapsed segments can also mimic pathological conditions.5–12 Thus, CT that involves oral administration of a large volume of contrast agent has been designed to distend the lumen for optimal visualization of the small intestines of humans. Computed tomography has also been used for examination of the gastrointestinal tract of dogs, but there are only a few reports13–15 of CT enterography of dogs.
The objective of the study reported here was to determine the necessity for luminal distention in the evaluation of the small intestines of dogs and to describe and optimize the techniques for CT enterography in clinically normal dogs. We hypothesized that the degree of luminal distention of the small intestines of dogs could be affected by variations in the methods for administration of contrast medium.
Materials and Methods
Animals
Fifteen client-owned clinically normal adult dogs were enrolled in the study. This included 13 adult dogs (age range, 1 to 7 years; body weight range, 2.3 to 6 kg). Six of the dogs were male (5 neutered) and 7 were female (2 neutered). Breeds represented included Poodle (n = 5), mixed (5), Shih Tzu (1), Beagle (1), and Pomeranian (1). Two additional dogs that underwent abdominal CT for evaluation of metastasis of mammary gland tumor were also included (a 5-year-old neutered female Maltese that weighed 3.6 kg and a 6-year-old sexually intact female Cocker Spaniel that weighed 6 kg). All dogs were clinically normal as determined on the basis of results of a physical examination, CBC, serum biochemical analysis, and measurement of electrolyte concentrations. No dogs had evidence of gastrointestinal disease on the basis of the medical history or results for abdominal radiography, ultrasonography, or fecal testing.
Owner informed consent was obtained for all dogs. The protocol for this study was approved by the Institutional Animal Care and Use Committee at Seoul National University.
CT enterography
A control group comprised 7 dogs (the 2 dogs that underwent abdominal CT for evaluation of metastasis of mammary gland tumor and 5 other volunteered dogs). Those 5 volunteered dogs then comprised a bolus administration group. Finally, the 8 other volunteered dogs comprised a continuous administration group.
Food was withheld from all dogs for 12 hours before CT examination. For the control group, anesthesia was induced with diazepama (0.2 mg/kg, IV) and propofolb (6 mg/kg, IV) and maintained with isofluoranec in oxygen. Computed tomography without lactulose administration was performed on the anesthetized dogs. Dogs of the bolus administration group were also anesthetized, and CT was performed without lactulose administration. After the initial CT was completed, gastric intubation with an 8F feeding tube was performed on each anesthetized dog. A lactulose solutiond (1.34 g/mL) was diluted at a ratio of 1:4 (1 part lactulose solution to 4 parts warm water) and was rapidly administered (total volume of the diluted solution administered, 60 mL/kg) via the orogastric tube. Butylscopolamine bromidee (0.4 mg/kg, IV) was administered with expectations that it would result in intestinal hypomotility, and CT was performed immediately thereafter. Computed tomography was performed 0, 10, 20, 30, 40, 50, and 60 minutes after bolus administration of lactulose solution. Dogs of the continuous administration group each received a nasoesophageal tube (3F to 5F). The lactulose solution was diluted at a ratio of 1:4 (1 part lactulose solution to 4 parts warm water) and was slowly administered (total volume of the diluted solution administered, 60 mL/kg) as a constant rate infusion via the nasoesophageal tube over a period of 45 minutes. Dogs were then anesthetized, butylscopolamine bromidee (0.4 mg/kg, IV) was administered, and CT was performed beginning 15 minutes after completion of lactulose solution administration.
All CT images were acquired with dogs positioned in sternal recumbency, with the head slightly elevated to prevent reflux of contrast agent from the stomach during CT examination. All CT images were acquired by use of a 16-channel multidetector CT scanner.f Images were acquired from the diaphragm to the pubic symphysis with the following settings: 120 kV, 200 mA, 1-second tube rotation time, 2.5-mm slice thickness, 1.375 pitch, and 200-mm field of view. Manual hyperventilation was performed during scanning to induce transient apnea and reduce motion artifacts. Adverse effects, including signs of nausea, vomiting, and diarrhea, were recorded.
Image analysis
The CT images were reconstructed at a thickness of 2.5 mm and evaluated with a soft tissue window (window width, 400 HUs; window level, 40 HUs) by 2 veterinary radiologists with ≥ 4 years of experience (SK and JS); the investigators were not aware of identifying information such as the group assignment or time at which the ST image was obtained. The small intestines were evaluated as the following 4 segments: descending duodenum, ascending duodenum, jejunum, and terminal ileum. The descending duodenum included the cranial duodenal flexure and descending portion of the duodenum. The ascending duodenum included the caudal duodenal flexure and ascending portion of the duodenum. The jejunum began at the duodenojejunal flexure and ended at the ileum. The terminal ileum was that portion of the ileum caudal to the ileocolic fold.
Luminal distention of each segment was qualitatively evaluated by use of a 3-point scale (0 = poor, 1 = good, and 2 = optimal) that had been modified from previous human enterography studies.9,16 The score was determined as the percentage of the small intestinal segment with adequate distention as follows: poor when < 40% of the segment was distended, good when 40% to 70% was distended, and optimal when > 70% was distended (Figure 1). During evaluation of the degree of luminal distention, the investigators attempted to examine the entire length of each given intestinal segment, if possible. The intestinal segment was considered to have adequate distention if the intestinal walls could be distinguished from the lumen.
Dorsal reconstructed CT images (window width, 400 HUs; window level, 40 HUs) of the jejunum of a clinically normal dog depicting qualitative evaluation of luminal distention by use of a 3-point scale (0, poor; 1, good; and 2, optimal). Images represent < 40% of the jejunal segment adequately distended (poor [A]), 40% to 70% of the jejunal segment adequately distended (good [B]), and > 70% of the jejunal segment adequately distended (optimal [C]).
Citation: American Journal of Veterinary Research 77, 4; 10.2460/ajvr.77.4.367
Statistical analysis
Age and body weight of dogs in the control, bolus administration, and continuous administration groups were compared by use of a 1-way ANOVA. Luminal distention scores were expressed as mean ± SD. Analysis of reproducibility between reviewers was performed by use of the ICC test. Luminal distention scores over time for the continuous administration group were analyzed by use of the Mann-Whitney U test. Values of P < 0.05 were considered significant. Statistical analyses were performed with commercial software.g
Results
Mean ± SD age of dogs did not differ significantly among the control (2.15 ± 2.71 years), bolus administration (3.63 ± 2.31 years), and continuous administration (3.11 ± 2.77 years) groups. Mean body weight did not differ among the control (4.04 ± 1.48 kg), bolus administration (3.81 ± 1.26 kg), and continuous administration (4.26 ± 1.44 kg) groups.
For the control group, luminal distention scores of all intestinal segments were poor. All intestinal segments of this group had luminal distention insufficient for detecting the intestinal wall (Figure 2).
Dorsal reconstructed CT images (window width, 400 HUs; window level, 40 HUs) of a representative dog of the control group that had poor luminal distention in the descending duodenum (A), ascending duodenum (B), jejunum (C), and terminal ileum (D). The descending duodenum included the cranial duodenal flexure and descending portion of the duodenum. The ascending duodenum included the caudal duodenal flexure and ascending portion of the duodenum. The jejunum began at the duodenojejunal flexure and ended at the ileum. The terminal ileum was that portion of the ileum caudal to the ileocolic fold. The intestinal wall is not clearly defined because the intestinal lumen (asterisk) is inappropriately distended.
Citation: American Journal of Veterinary Research 77, 4; 10.2460/ajvr.77.4.367
For the bolus administration group, mean ± SD luminal distention scores for the 2 investigators for each intestinal segment at each time point were summarized (Table 1). The highest luminal distention score for the descending duodenum was at 20 minutes, and the highest score for the ascending duodenum was at 40 minutes, for the jejunum was at 30 and 40 minutes, and for the terminal ileum was at 60 minutes (Figure 3). Interobserver reproducibility was high (ICC, 0.872 to 0.982) for all intestinal segments. Mean ± SD luminal distention scores for the entire small intestine of the bolus administration group were summarized (Table 2).
Dorsal reconstructed CT images (window width, 400 HUs; window level, 40 HUs) of a representative dog of the bolus administration group obtained at 20 minutes for the descending duodenum (A), 40 minutes for the ascending duodenum (B), 40 minutes for the jejunum (C), and 60 minutes for the terminal ileum (D). The intestinal lumen (asterisk) had good distention in the descending duodenum, ascending duodenum, and jejunum but poor distention in the terminal ileum. See Figure 2 for remainder of key.
Citation: American Journal of Veterinary Research 77, 4; 10.2460/ajvr.77.4.367
Luminal distention score* and ICC for each intestinal segment for the bolus administration group (n = 5 dogs) on the basis of time after administration of lactulose solution.
| Time (min)† | ||||||||
|---|---|---|---|---|---|---|---|---|
| Intestinal segment‡ | 0 | 10 | 20 | 30 | 40 | 50 | 60 | ICC |
| Descending duodenum | 0.70 ± 0.67 | 1.20 ± 0.42 | 1.30 ± 0.48 | 1.20 ± 0.63 | 1.10 ± 0.73 | 1.10 ± 0.99 | 0.90 ± 0.87 | 0.955 |
| Ascending duodenum | 0.60 ± 0.84 | 1.10 ± 0.87 | 1.40 ± 0.51 | 1.50 ± 0.52 | 1.60 ± 0.51 | 1.40 ± 0.51 | 1.30 ± 0.82 | 0.943 |
| Jejunum | 0.10 ± 0.31 | 0.60 ± 0.51 | 0.70 ± 0.67 | 1.00 ± 0.94 | 1.00 ± 0.94 | 0.90 ± 0.73 | 0.90 ± 0.73 | 0.982 |
| Terminal ileum | 0 ± 0 | 0 ± 0 | 0 ± 0 | 0 ± 0 | 0 ± 0 | 0 ± 0 | 0.40 ± 0.84 | 0.872 |
Values reported represent the mean ± SD for 2 investigators who scored luminal distention by use of a 3-point scale (0, poor [< 40% of the jejunal segment adequately distended]; 1, good [40% to 70% of the jejunal segment adequately distended]; and 2, optimal [> 70% of the jejunal segment adequately distended]).
Oral administration of a bolus (60 mL/kg) of lactulose solution (1.34 g/mL) diluted 1:4 was designated as time 0.
The descending duodenum included the cranial duodenal flexure and descending portion of the duodenum. The ascending duodenum included the caudal duodenal flexure and ascending portion of the duodenum. The jejunum began at the duodenojejunal flexure and ended at the ileum. The terminal ileum was that portion of the ileum caudal to the ileocolic fold.
Luminal distention score* and ICC of the entire small intestinal tract for the bolus administration group (n = 5 dogs) and the continuous administration group (8) on the basis of time after administration of lactulose solution.
| Time (min)† | ||||||||
|---|---|---|---|---|---|---|---|---|
| Administration group | 0 | 10 | 20 | 30 | 40 | 50 | 60 | ICC |
| Bolus | 0.35 ± 0.62 | 0.73 ± 0.71 | 0.85 ± 0.73 | 0.93 ± 0.82 | 0.93 ± 0.85 | 0.85 ± 0.83 | 0.88 ± 0.85 | 0.953 |
| Continuous | 1.34 ± 0.78 | 1.38 ± 0.70 | 1.38 ± 0.74 | 1.25 ± 0.77 | 1.19 ± 0.77 | 1.19 ± 0.73 | 1.08 ± 0.71 | 0.927 |
Oral administration of a bolus (60 mL/kg) of lactulose solution (1.34 g/mL) diluted 1:4 was designated as time 0 for the bolus group; time 0 for the continuous group was 15 minutes after completion of a continuous oral administration of the same total dose of lactulose solution, which was administered over a 45-minute period.
See Table 1 for remainder of key.
For the continuous administration group, mean ± SD luminal distention scores for the 2 investigators for each intestinal segment at each time point were summarized (Table 3). The descending duodenum had the highest luminal distention score at 0 minutes, and the highest score for the ascending duodenum was at 10 and 30 minutes, for the jejunum was at 20 minutes, and for the terminal ileum was at 20 to 60 minutes (Figure 4). Interobserver reproducibility was high (ICC, 0.896 to 0.951) for all intestinal segments. Mean ± SD luminal distention scores for the entire small intestine of the continuous administration group were summarized (Table 2). Luminal distention scores from 0 to 20 minutes were significantly higher than scores from 30 to 60 minutes.
Dorsal reconstructed CT images (window width, 400 HUs; window level, 40 HUs) of a representative dog of the continuous administration group obtained at 0 minutes for the descending duodenum (A), 10 minutes for the ascending duodenum (B), 20 minutes for the jejunum (C), and 30 minutes for the terminal ileum (D). The intestinal lumen (asterisk) had good distention in all small intestinal segments. See Figure 2 for remainder of key.
Citation: American Journal of Veterinary Research 77, 4; 10.2460/ajvr.77.4.367
Luminal distention score* and ICC for each intestinal segment for the continuous administration group (n = 8 dogs) on the basis of time after administration of lactulose solution.
| Time (min)† | ||||||||
|---|---|---|---|---|---|---|---|---|
| Intestinal segment‡ | 0 | 10 | 20 | 30 | 40 | 50 | 60 | ICC |
| Descending duodenum | 1.63 ± 0.71 | 1.56 ± 0.51 | 1.50 ± 0.51 | 1.13 ± 0.71 | 1.06 ± 0.68 | 1.25 ± 0.44 | 1.06 ± 0.44 | 0.951 |
| Ascending duodenum | 1.56 ± 0.62 | 1.63 ± 0.61 | 1.56 ± 0.72 | 1.63 ± 0.61 | 1.50 ± 0.63 | 1.38 ± 0.71 | 1.19 ± 0.75 | 0.916 |
| Jejunum | 1.38 ± 0.50 | 1.38 ± 0.50 | 1.44 ± 0.51 | 1.25 ± 0.57 | 1.19 ± 0.65 | 1.13 ± 0.61 | 1.06 ± 0.57 | 0.896 |
| Terminal ileum | 0.81 ± 0.98 | 0.94 ± 0.92 | 1.00 ± 1.03 | 1.00 ± 1.03 | 1.00 ± 1.03 | 1.00 ± 1.03 | 1.00 ± 1.03 | 0.945 |
Time 0 was 15 minutes after completion of a continuous oral administration of lactulose solution (60 mL/kg), which was administered over a 45-minute period.
See Table 1 for remainder of key.
From 1 hour before to 1 hour after CT examination (as well as throughout the CT examination), 5 of 8 dogs in the continuous administration group had signs of nausea, 5 of 8 vomited, and 3 of 8 were diarrheic. Clinical signs resolved without treatment within 24 hours.
Discussion
In veterinary medicine, hydro-CT for stomach images14 or gastrointestinal CT images15 has been described. In a study14 involving hydro-CT, the stomach wall before administration of water was not appropriate for evaluation because the lumen was empty and collapsed. Computed tomographic evaluation of the gastric wall was performed after administration of various volumes of water via gastric tube, and it was proposed that oral administration of 30 mL of water/kg with IV administration of a contrast agent was adequate for uniform gastric distention and assessment of the stomach wall.14 In another CT study15 of 19 dogs without luminal distention, the gastrointestinal wall was identified from gastrointestinal segments in 77.7% of all gastrointestinal segments.
In the study reported here, the control group had poor distention of all small intestinal segments. General CT of the small intestines may not be appropriate for evaluating the intestinal wall because of poor distention of the lumen; adequate luminal distention is a requirement for CT examination of the small intestines of dogs, similar to the situation for humans.17 Results for the present study differed from those of a previous report15 in which there was a high rate for identification of the gastrointestinal wall without oral administration of contrast medium. We suspect that the lumen of certain intestinal segments was unevenly filled with gas or fluid (or both), and intestinal segments that are not fully distended may be inappropriate for the accurate evaluation of changes of the intestinal wall.
Computed tomographic examination of the small intestines of humans can be broadly classified into enteroclysis and enterography, depending on the method of contrast agent administration.10,17,18 Computed tomographic enteroclysis is a technique that involves administration of contrast material directly into the lumen of the jejunum by placing a nasojejunal feeding tube at the duodenojejunal junction via fluoroscopic guidance. Although this method provides good distention of the jejunal loops, CT enteroclysis is invasive and inconvenient and causes patient discomfort.5,7,10,18–20 Computed tomographic enterography is emerging as an alternative method for the assessment of small bowel disease. Computed tomographic enterography is relatively noninvasive and more convenient than is CT enteroclysis because it involves oral administration of a contrast agent without nasojejunal tube placement.5,10,18
In the present study, we modified the human CT enterography technique for distending the small intestinal lumen. Our modifications accounted for noninvasiveness and feasibility. The protocol for CT enterography has not been standardized for humans. Various orally administered neutral contrast agents (eg, water, water and methylcelluose, lactulose solution, ultra–low-dose barium, polyethylene glycol, and milk) have been evaluated for their ability to improve small bowel distention for CT enterography of humans.8,9,11,19,21,22 Lactulose solution reportedly is an effective, orally administered neutral contrast agent for humans because it links unabsorbed, unfermented lactulose molecules with water.9 The volume of lactulose solution used in the present study (60 mL/kg) was determined on the basis of results for preliminary experiments in which we detected appropriate overall small intestinal distention. In 1 preliminary experiment, a lactulose solution (1.34 g/mL) diluted at a ratio of 1:4 (total dose administered, 30 mL/kg) that was continuously administered provided poor luminal distention in the duodenum, uneven luminal distention in the jejunum, and optimal luminal distention in the ileum. In another preliminary experiment, a lactulose solution (1.34 g/mL) diluted at a ratio of 1:4 (total dose administered, 70 mL/kg) that was continuously administered provided good luminal distention throughout the small intestines, but there were signs of severe nausea.
Although adverse effects for CT enterography with lactulose in humans have been detected only in geriatric patients or in patients with malignancies, mild gastrointestinal signs were evident in healthy dogs in the continuous administration group in the study reported here. Overloading nonanesthetized dogs with a large volume of liquid over a relatively prolonged period was suspected to be the cause of the signs of nausea and vomiting, but more studies are needed to determine the optimal total volume and dilution rate for lactulose solution, and caution is needed to prevent aspiration pneumonia.
In humans, contrast agent is orally administered by voluntary drinking. The total volume is divided, and portions are ingested several times during a 30- to 75-minute period for a more even distribution throughout the intestinal tract.21,23–25 Two methods for oral administration of a large dose of contrast agent were used in the present study. Because it is not possible to induce voluntary drinking of contrast agent by dogs, a large volume of lactulose solution was administered as a bolus to anesthetized dogs. Although there was good luminal distention in the ascending duodenum, descending duodenum, and jejunum during the first 60 minutes after bolus administration, the terminal ileum had poor luminal distention at all time points. For humans, continuous oral intake during a 15- to 20-minute period is required for successful intestinal distention, compared with discontinuous intake or intake over a more prolonged time frame.10 For more effective luminal distention of all small intestinal segments in the present study, the same total dose of lactulose solution was provided via continuous administration during a 45-minute period before induction of anesthesia. Examination of the CT image obtained 15 minutes after induction of anesthesia revealed that all small intestinal segments had good luminal distention during the first 60 minutes, except for the images of the terminal ileum obtained at 0 and 10 minutes. As a result, we concluded that continuous oral administration of contrast agent is required for a more even distribution in the intestinal lumen for CT enterography of dogs, similar to the situation for humans. The time at which the CT image with the greatest luminal distention was obtained for all small intestinal segments typically was 10 and 20 minutes for the continuous administration group. The degree of distention of the small intestine differed between the 2 administration methods, which was in agreement with our hypothesis. Although the adverse effects were mild for the continuous administration group, care must be taken during anesthetic recovery.
Butylscopolamine bromide was administered immediately before CT in the present study. We anticipated that the butylscopolamine bromide would cause stagnation of luminal contents because of intestinal hypomotility. Although the spasmolytic effect of butylscopolamine bromide in dogs has been examined,26 the effect of butylscopolamine bromide on luminal distention is not clear and more studies are needed. Prokinetic agents such as glucagon, hyoscine-N-butylbromide, or metoclopramide are sometimes used in conjunction with oral administration of contrast agents to humans for maximizing bowel distention with a minimum amount of contrast intake, but the usefulness of these drugs has not been clearly identified.9,11,18,23,24
In the present study, the CT enterography technique of administering a lactulose solution (1.34 g/mL) diluted at a ratio of 1:4 (total dose administered, 60 mL/kg) via continuous oral administration over a 45-minute period through a nasoesophageal tube provided good distention of all small intestinal segments, with the greatest luminal distention detected between 0 and 20 minutes after lactulose administration was completed. These data can be used for additional CT enterography studies on bowel disease of dogs. Computed tomographic enterography can be used in the evaluation of small bowel disease (eg, inflammatory or neoplastic disease) for detection of mural thickening, symmetry of small bowel thickening, and mucosal hyperenhancement after IV administration of contrast agent. To standardize CT enterography protocols for use on dogs, further studies are needed regarding the technique of continuous oral administration of a large volume of contrast agent. Additionally, factors that can affect the degree of luminal distention and quality of images; the types, amounts, and dilution rates of contrast agents; the use of prokinetic agents; and CT imaging time and image-acquisition intervals need to be further evaluated.
Acknowledgments
Presented at the 2014 Annual Scientific Conference of the American College of Veterinary Radiology, St Louis, October 2014.
ABBREVIATIONS
| HU | Hounsfield unit |
| ICC | Intraclass correlation coefficient |
Footnotes
Merode, Dong Wha Pharm Corp, Seoul, Korea.
Pofol, Dongkook Corp, Seoul, Korea.
Terrell, Piramal Critical Care Inc, Bethlehem, Pa.
Duphalac syrup, JW Pharmaceutical Corp, Seoul, Korea.
Buscopan, Boehringer Ingelheim Vetmedica Inc, St Joseph, Mo.
GE LightSpeed 16, GE Healthcare, Fairfield, Conn.
SPSS for Windows, release 22.0, standard version, SPSS Inc, Chicago, Ill.
References
1. Brizi MG, Minordi L, Mirk P, et al. The state of the art of small bowel imaging: combine the old with the new. Rays 2002; 27: 51–65.
2. Burns J, Fox SM. The use of a barium meal to evaluate total gastric emptying time in the dog. Vet Radiol 1986; 27: 169–172.
3. Penninck DG, Nyland TG, Fisher PE, et al. Ultrasonography of the normal canine gastrointestinal tract. Vet Radiol 1989; 30: 272–276.
4. Penninck DG, Nyland TG, Kerr LY, et al. Ultrasonographic evaluation of gastrointestinal diseases in small animals. Vet Radiol 1990; 31: 134–141.
5. Elsayes KM, Al-Hawary MM, Jagdish J, et al. CT enterography: principles, trends, and interpretation of findings. Radiographics 2010; 30: 1955–1970.
6. Macari M, Balthazar EJ. CT of bowel wall thickening: significance and pitfalls of interpretation. AJR Am J Roentgenol 2001; 176: 1105–1116.
7. Macari M, Megibow AJ, Balthazar EJ. A pattern approach to the abnormal small bowel: observations at MDCT and CT enterography. AJR Am J Roentgenol 2007; 188: 1344–1355.
8. Paulsen SR, Huprich JE, Fletcher JG, et al. CT Enterography as a diagnostic tool in evaluating small bowel disorders: review of clinical experience with over 700 cases. Radiographics 2006; 26: 641–657.
9. Arslan H, Etlik O, Kayan M, et al. Peroral CT enterography with lactulose solution: preliminary observations. AJR Am J Roentgenol 2005; 185: 1173–1179.
10. Paparo F, Garlaschi A, Biscaldi E, et al. Computed tomography of the bowel: a prospective comparison study between four techniques. Eur J Radiol 2013; 82:e1–e10.
11. Wold PB, Fletcher JG, Johnson CD, et al. Assessment of small bowel Crohn disease: noninvasive peroral CT enterography compared with other imaging methods and endoscopy feasibility study. Radiology 2003; 229: 275–281.
12. Young BM, Fletcher JG, Booya F, et al. Head-to-head comparison of oral contrast agents for cross-sectional enterography: small bowel distention, timing, and side effects. J Comput Assist Tomogr 2008; 32: 32–38.
13. Raptopoulos V, Davis M, Smith E. Imaging of the bowel wall. Computed tomography and fat density oral-contrast agent in an animal model. Invest Radiol 1986; 21: 847–850.
14. Terragni R, Vignoli M, Rossi F, et al. Stomach wall evaluation using helical hydro-computed tomography. Vet Radiol Ultrasound 2012; 53: 402–405.
15. Hoey S, Drees R, Hetzel S. Evaluation of the gastrointestinal tract in dogs using computed tomography. Vet Radiol Ultrasound 2013; 54: 25–30.
16. Minowa O, Ozaki Y, Kyogoku S, et al. MR imaging of the small bowel using water as a contrast agent in a preliminary study with healthy volunteers. AJR Am J Roentgenol 1999; 173: 581–582.
17. Minordi LM, Vecchioli A, Mirk P, et al. CT enterography with polyethylene glycol solution vs CT enteroclysis in small bowel disease. Br J Radiol 2011; 84: 112–119.
18. Ilangovan R, Burling D, George A. CT enterography: review of technique and practical tips. Br J Radiol 2012; 85: 876–886.
19. Maglinte DD, Sandrasegaran K, Lappas JC, et al. CT enteroclysis. Radiology 2007; 245: 661–671.
20. Lauenstein TC, Schneemann H, Vogt FM, et al. Optimization of oral contrast agents for MR imaging of the small bowel. Radiology 2003; 228: 279–283.
21. Bodily KD, Fletcher JG, Solem CA, et al. Crohn disease: mural attenuation and thickness at contrast-enhanced CT enterography—correlation with endoscopic and histologic findings of inflammation. Radiology 2006; 238: 505–516.
22. Kung CH, Wang HJ, Leung TK, et al. Depiction of bowel wall visualization and dilation in abdominopelvic MDCT: comparison of high-attenuation contrast medium, water and whole milk. J Exp Clin Med 2010; 2: 186–191.
23. Megibow AJ, Babb JS, Hecht EM, et al. Evaluation of bowel distention and bowel wall appearance by using neutral oral contrast agent for multi-detector row CT. Radiology 2006; 238: 87–95.
24. Hara AK, Leighton JA, Heigh RI, et al. Crohn disease of the small bowel: preliminary comparison among CT enterography, capsule endoscopy, small-bowel follow-through, and ileoscopy. Radiology 2006; 238: 128–134.
25. Colombel JF, Solem CA, Sandborn WJ, et al. Quantitative measurement and visual assessment of ileal Crohn's disease activity by computed tomography enterography: correlation with endoscopic severity and C reactive protein. Gut 2006; 55: 1561–1567.
26. Sagrada A, Schiavone A, Cefalá A, et al. N-butyl hyoscine exerts local spasmolytic effect in the small and large bowel of the conscious dog. Arch Int Pharmacodyn Ther 1987; 287: 237–247.
