Computed tomographic enterography is a noninvasive method that can be used to accurately evaluate small bowel lesions and extraenteric structures.1 It is performed by dilating the lumen of the gastrointestinal tract with an orally administered contrast agent and then enhancing the intestinal wall and mesenteric vessels by IV administration of a contrast agent. Protocols for CT enterography have been evaluated in humans with regard to contrast agents (type, dose, dilution ratio, and administration method), drugs for modulating gastrointestinal motility, IV administration of contrast agent (concentration and dose), and scan timing.1–6 In veterinary medicine, only a few studies2,7–9 have been performed with CT enterography, and those studies focused on the volume of orally administered contrast agent or scan timing.
For CT enterography in humans, the mural contrast enhancement pattern, length and location of lesions in the small bowel wall, and involvement of mesenteric vessels are usually assessed.3,10 When obscure gastrointestinal bleeding, bowel stricture, and vascular occlusion such as a thrombus or small bowel neoplasia are suspected, mesenteric circulation and enhancement of the small bowel wall are evaluated. In general, mesenteric circulation is assessed in the arterial phase to determine the degree of enhancement, distribution, and visualization of vascular branches, whereas enhancement of the small bowel wall is evaluated in the venous phase.3,10,11
A split-bolus technique combines the arterial and venous phases into 1 CT image after the total dose of the contrast agent is split and administered as 2 injections. This technique decreases radiation exposure to the patient and reduces the total number of CT images that must be interpreted, compared with radiation exposure and the number of images required for dual-phase scanning.12–16 Split-bolus techniques have not been widely applied in CT enterography, even in human medicine. However, in a retrospective study16 of 66 humans with active inflammatory bowel diseases, this technique allowed a significantly higher rate of detection of mucosal hyperenhancement, compared with the detection rate for single-injection CT enterography.
The purpose of the study reported here was to investigate the use of split-bolus CT enterography for the evaluation of the intestinal wall and mesenteric vessels in healthy dogs. We hypothesized that split-bolus CT enterography could be performed in dogs and would provide enhancement of the small intestinal wall and mesenteric vessels similar to that of dual-phase CT enterography.
Materials and Methods
Animals
Six sexually intact male Beagles were used in the study. Median age was 2 years (range, 1 to 3 years), and median body weight was 11.7 kg (range, 9.3 to 14.2 kg). All dogs were deemed healthy on the basis of results of a physical examination, auscultation, blood pressure measurement, CBC, blood biochemical analysis, thoracic and abdominal radiography, echocardiography, and abdominal ultrasonography. The study protocol was approved by the Institutional Animal Care and Use Committee at Chonnam National University (protocol No. YB-2018-45). Dogs were cared for in accordance with the guidelines for animal experiments of Chonnam National University.
Preparation for CT enterography
A nonrandomized crossover study was conducted. Food was withheld from each dog for 36 hours. At least 12 hours before dogs were anesthetized for imaging, 250 mL of polyethylene glycol solutiona was administered orally with a gastric tube to evacuate the gastrointestinal tract. Immediately before anesthesia was induced, lactulose (1.34 g/mL) was diluted with water (1 part lactulose to 4 parts water), and 2 doses of dilute lactulose solution (30 mL/kg for each dose) were orally administered 20 minutes apart to each dog via a gastric tube. Anesthesia was induced by administration of alfaxaloneb (2 mg/kg, IV) and maintained with isofluranec in oxygen (1 L/min). Butylscopolamine bromided (0.4 mg/kg, IV) was administered immediately before CT enterography to induce intestinal hypomotility.
The CT images were obtained 20 minutes after the second dose of the lactulose solution was administered, with the dogs positioned in sternal recumbency. Intravenous administration of contrast agent was performed in accordance with the CT enterography protocol. All CT images were acquired by use of a 16-row multidetector CT scannere with the following settings: slice thickness = 1 mm, pitch = 0.8, rotation duration = 600 milliseconds, tube voltage = 120 kV, and tube current = 120 mA. Dogs were hyperventilated to induce apnea immediately before image acquisition to minimize motion artifacts. Blood pressure, heart rate, and respiratory rate of the dogs were monitored during CT enterography. After CT enterography was completed and for 5 days, each dog was monitored for general condition and adverse effects such as vomiting, lethargy, and anorexia.
CT enterography protocol
In 3 sessions separated by a 7-day period, each dog underwent CT enterography by means of a different enterography technique in the following order: dual-phase enterography with a test bolus and 2 techniques involving a split dose of contrast agent (split enterography with a test bolus [split technique] and split enterography with bolus tracking [split-bolus tracking technique]; Appendix 1).
Prior to performance of CT enterography with the dual-phase and split techniques, a test bolus was used to determine the scan delay appropriate for use. Precontrast helical CT images were first obtained, and then a test bolus of iohexolf (0.5 mL/kg) was injected with a power injectorg (rate, 3 mL/s) via a 22-gauge catheter inserted in a cephalic vein. Subsequently, CT images were obtained at the level of the aorta where it branched to the cranial mesenteric artery. On the basis of evaluation of time-to-attenuation curves for the aorta and portal vein, the scan delay of the arterial phase was determined as 7 seconds (time to 15% of the peak enhancement), and scan delay of the venous phase was determined as 20 seconds (time to reach peak enhancement). Immediately after the test bolus scan, dual-phase CT enterography was performed. Iohexol (2 mL/kg, IV) was injected with the power injector (rate, 3 mL/s). Arterial-phase CT images were obtained from the cranial region of the transverse colon to the pelvis, and venous-phase CT images were obtained from the diaphragm to the pelvis.
For the split technique, the same total dose of iohexol (2 mL/kg) was used as for the dual-phase technique. However, 60% of the total dose of contrast agent was injected at 0 seconds, followed by injection of the remaining 40% of the total dose of contrast agent at 13 seconds, which was the time difference between the arterial scan delay and venous scan delay. A single set of CT images was obtained at 20 seconds after the first contrast agent injection, representing the time when the first injection of contrast agent reached the venous phase and the second injection of contrast agent reached the arterial phase.
For the split-bolus tracking technique, an iohexol dose of 2.5 mL/kg was used because no test bolus (0.5 mL/kg) was injected. Accordingly, 60% of the total dose of the contrast agent was injected at 0 seconds, followed by injection of the remaining 40% at 13 seconds, which was the previously identified time difference between the arterial scan delay and venous scan delay. Only a single set of CT images was obtained; acquisition of the CT images was initiated when contrast enhancement of the aorta reached 100 HU at the trigger point where the aorta branched to the cranial mesenteric artery, as determined by use of a bolus tracking program.h
All acquired CT images were reconstructed with a slice thickness of 1 mm, interval of 1 mm, and soft kernel frequency. Images then were reformatted into multiplanar reconstructions and maximum intensity projections.
Evaluation of CT images
All CT images were evaluated at a work station separately by 2 reviewers (KCH and LSK), who used a picture archiving and communication systemi with a window width of 400 HU and window level of 40 HU. The reviewers were not aware of the enterographic procedure used to obtain the CT images.
Qualitative evaluation included assessment of the visibility of peripheral vascularity, enhancement patterns of the intestine, and CT image quality including artifacts (Appendix 2). Visibility of the peripheral vascularity was assessed by evaluating the arterial arcade (arch-like structure made by a series of anastomosing arterial branches in the mesentery) and vasa recta (straight arteries arising from the arcades) of the cranial mesenteric artery to the corresponding intestinal loops on maximum intensity projections for the dorsal plane (Figure 1). Enhancement of the intestinal wall was evaluated at 3 sites: the duodenum immediately caudal to the cranial duodenal flexure, the most enhanced segment of jejunum at the level of the caudal pole of the left kidney, and the terminal 2 cm of the ileum. Margination of the intestinal wall was assessed on the basis of visual examination of the serosal surface of the intestinal wall.
Dorsal plane (A through C) and transverse (D through G) maximum intensity projection reconstruction CT enterography images of healthy Beagles depicting qualitative assessment of mesenteric peripheral vascularity and bowel wall enhancement. Mesenteric peripheral vascularity was evaluated on dorsal plane images, revealing the arch-like structure (ie, arcade) of the cranial mesenteric artery (arrows in panel A), the arcade (long black arrows) and vasa recta (short black arrows; both somewhat visible in panel B), and the arcade (long black arrows) and vasa recta (short black arrows; both markedly visible in panel C). Bowel wall enhancement was evaluated on transverse images, revealing the artery within the intestinal wall (arrowheads in panel D), an enhanced mucosal layer (arrowheads in panel E), transmural enhancement of the bowel wall (F), and transmural enhancement with a hyperattenuated mucosal layer (arrows in panel G).
Citation: American Journal of Veterinary Research 81, 2; 10.2460/ajvr.81.2.122
For quantitative evaluations, the degree of attenuation (HU) of the portal vein, cranial mesenteric artery, and cranial mesenteric vein was measured on the precontrast, arterial phase, and venous phase images by placing circular regions of interest (1.0 to 2.5 mm2) in the center of vessels to avoid perivascular structures. Attenuation of the portal vein was measured at the level where the aorta branched to the celiac artery. Attenuation of the cranial mesenteric artery and vein was measured at the level where the aorta and portal vein branched, respectively. Attenuation of intestinal walls was measured in the duodenum, jejunum, and ileum at the same sites used for the qualitative assessment by use of defined circular regions of interest (1.0 to 2.5 mm2; Figure 2). The difference in attenuation of the intestinal walls between the precontrast and postcontrast images was calculated for each site. The contrast-to-noise ratio was calculated as follows: (mean intestinal wall attenuation – mean gluteal muscle attenuation)/SD of air.
Transverse CT enterography image of a healthy Beagle with placement of a region of interest (circle) that included all mucosal layers and was used for evaluation of attenuation of the intestinal wall.
Citation: American Journal of Veterinary Research 81, 2; 10.2460/ajvr.81.2.122
Statistical analysis
Data were reported as mean ± SD. Differences among the 3 CT enterography techniques in qualitative and quantitative factors was evaluated by use of ANOVA. Differences among techniques in visualization scores for qualitative values (eg, peripheral vascularity, image quality, and intestinal wall enhancement) and enhancement scores for quantitative values (eg, small intestinal wall, mesenteric vessels, and contrast-to-noise ratio), total number of CT images, and scan times were evaluated by use of the Kruskal-Wallis test with the Bonferroni correction. Agreement between reviewers was analyzed by use of the intraclass correlation coefficient. Values were considered significant at P < 0.05. All analyses were performed with statistical software.j
Results
All CT enterography images were obtained from all dogs without complications (eg, vomiting or diarrhea). The number of total images required for interpretation was significantly (P = 0.013) lower for the split technique than for the other 2 techniques. The mean ± SD total number of CT images by use of each protocol was 620.33 ± 24.08 images/dog for the dual-phase technique, 288.16 ± 10.38 images/dog for the split technique, and 317 ± 47.25 images/dog for the split-bolus tracking technique. The scan time for CT enterography was significantly (P = 0.025) less for the split-bolus tracking technique than for the other 2 techniques. The time from acquisition of the precontrast images until CT enterography was completed was less for the split-bolus tracking technique (median, 58 seconds) than for the split technique (131 seconds) or the dual-phase technique (152 seconds).
Enhancement of mesenteric vessels to the periphery, including the arcade and vasa recta, was identified, and contrast enhancement of the intestinal wall was distinctly observed on CT enterography in each dog for all 3 techniques. The split technique provided the most enhancement of intestinal wall images, compared with enhancement for the dual-phase and split-bolus tracking techniques (Figure 3).
Maximum intensity projection reconstruction (A through C) and multiplanar reconstruction (D through F) CT enterography images for evaluation of enhancement of mesenteric vessels in healthy Beagles by use of a dual-phase technique (A and D), split technique (B and E), and split-bolus tracking technique (C and F). In panels D, E, and F, the mesenteric vessels, such as the arcade (long arrows) and vasa recta (short arrows), are visible in the periphery of images obtained with all 3 techniques.
Citation: American Journal of Veterinary Research 81, 2; 10.2460/ajvr.81.2.122
For the qualitative evaluation, the mesenteric vascularity was markedly visible on CT enterography with all contrast techniques. Visualization of the mesenteric vascularity was not significantly different among the techniques (mean ± SD score, 2.75 ± 0.45 for the arterial phase and 2.75 ± 0.45 for the venous phase of the dual-phase technique, 2.58 ± 0.51 for the split technique, and 2.41 ± 0.51 for the split-bolus tracking technique). Scores for enhancement of the intestinal wall differed on the basis of the evaluated sites (Table 1). Visualization scores for the duodenal wall were significantly lower for the split and split-bolus tracking techniques than for the arterial phase (P = 0.017) and venous phase (P = 0.005) of the dual-phase technique. Visualization of the ileal wall for the split technique was similar to that in the venous phase of the dual-phase technique; however, visualization scores for the ileum were significantly (P = 0.025) lower with the split-bolus tracking technique. In the jejunum, there was no significant difference among CT enterography techniques. Enhancement patterns of the intestine differed among CT enterography techniques. For the dual-phase technique, various contrast patterns (eg, arterial, mucosal, transmural, or transmural enhancement with higher mucosal attenuation) were observed in the arterial phase. In the venous phase, transmural enhancement of the intestinal wall became homogeneous regardless of the evaluated site. For the split technique, only the transmural contrast pattern was observed in the duodenum, jejunum, and ileum (Figure 4); however, the serosal surface of the intestinal wall was more markedly visible for the split technique than for the other techniques, and clear margination of the intestinal wall was provided at all evaluated sites (Figure 5). For the split-bolus tracking technique, most sites had a transmural enhancement pattern; however, in some regions (2 duodenum, 1 jejunum, and 1 ileum), only the mucosal layer was enhanced. All 3 techniques provided optimal image quality in all dogs, with mean ± SD scores of 3.00 ± 0.00 for the arterial phase and 2.91 ± 0.28 for the venous phase of the dual-phase technique, 2.91 ± 0.28 for the split technique, and 3.00 ± 0.00 for the split-bolus tracking technique. There was no artifact associated with the contrast agent.
Mean ± SD score for qualitative evaluation of enhancement of the intestine of 6 healthy Beagles during CT enterography performed with 3 contrast techniques.
| Dual phase | ||||
|---|---|---|---|---|
| Location | Arterial phase | Venous phase | Split | Split-bolus tracking |
| Duodenum | 3.08 ± 0.90a | 3.00 ± 0.00a | 2.58 ± 0.5b | 2.41 ± 0.5b |
| Jejunum | 3.00 ± 0.85 | 3.00 ± 0.00 | 3.00 ± 0.00 | 2.83 ± 0.57 |
| Ileum | 2.91 ± 0.79a | 3.00 ± 0.00b | 3.00 ± 0.00b | 2.91 ± 0.28a |
Within a row, values with different superscript letters differ significantly (P < 0.05).
Transverse CT enterography images of the duodenum in healthy Beagles obtained during the arterial (A) and venous (B) phase of the dual-phase technique (B), by use of the split technique (C), and by use of the split-bolus tracking technique (D). Transmural enhancement with high mucosal attenuation (long arrows) is evident in the arterial phase of the dual-phase technique (A), whereas transmural enhancement (short arrows) is evident during the venous phase of the dual-phase technique (B) and with the other 2 techniques (C and D). Images were obtained with the following settings: slice thickness = 1 mm, interval = 1 mm, soft kernel frequency, window width = 400 HU, and window level = 40 HU.
Citation: American Journal of Veterinary Research 81, 2; 10.2460/ajvr.81.2.122
Dorsal plane multiplanar reconstruction CT images of the duodenum in healthy Beagles obtained during the arterial (A) and venous (B) phases of the dual-phase technique, by use of the split technique (C), and by use of the split-bolus tracking technique (D) for CT enterography. The serosal surface of the intestinal wall (arrows in panel C) is more markedly visible, and there is clearer margination of the intestinal wall with the split technique than with the other techniques.
Citation: American Journal of Veterinary Research 81, 2; 10.2460/ajvr.81.2.122
For the quantitative evaluation, mean attenuation of the cranial mesenteric artery in the arterial phase of the dual-phase technique was significantly higher than mean attenuation of this artery for the split technique or split-bolus tracking technique (Table 2). Compared with mean attenuation of the portal vein and cranial mesenteric vein in the venous phase of the dual-phase technique, mean attenuation for the split technique was statistically similar and for the split-bolus tracking technique was significantly lower. Attenuation of the enhanced intestinal wall was not significantly different among techniques in the duodenum and jejunum, but attenuation in the ileum was significantly (P = 0.008) higher for the split technique than for the dual-phase or split-bolus tracking techniques (Table 3).
Mean ± SD attenuation (HU) of mesenteric vessels for 6 healthy Beagles as determined by use of CT enterography with 3 contrast techniques.
| Dual phase | ||||
|---|---|---|---|---|
| Vessel | Arterial phase | Venous phase | Split | Split-bolus tracking |
| Portal vein | 24.85 ± 14.63 | 165.96 ± 20.57a | 154.24 ± 27.62a | 133.42 ± 29.53b |
| Cranial mesenteric artery | 451.01 ± 77.75a | 158.42 ± 38.14 | 293.39 ± 48.83b | 169.43 ± 66.23b |
| Cranial mesenteric vein | 16.26 ± 12.39 | 159.64 ± 20.26a | 155.56 ± 31.13a | 118.79 ± 31.13b |
See Table 1 for key.
Mean ± SD attenuation (HU) of the enhanced intestinal wall of 6 healthy Beagles as determined by use of CT enterography with 3 contrast techniques.
| Dual phase | ||||
|---|---|---|---|---|
| Location | Arterial phase | Venous phase | Split | Split-bolus tracking |
| Duodenum | 65.96 ± 39.38 | 66.16 ± 11.39 | 82.71 ± 20.01 | 75.08 ± 23.64 |
| Jejunum | 77.52 ± 62.23 | 68.37 ± 18.95 | 73.25 ± 11.25 | 71.83 ± 14.91 |
| Ileum | 42.71 ± 25.21a | 60.21 ± 13.69a | 71.16 ± 11.00b | 55.24 ± 13.98a |
See Table 1 for key.
The mean ± SD contrast-to-noise ratio was generally higher for the dual-phase technique (6.39 ± 5.86 in the arterial phase and 6.10 ± 5.72 in venous phase) than for the split-bolus technique (5.06 ± 3.05) and split-bolus tracking technique (5.31 ± 3.14). However, there was no significant difference in these values among the 3 techniques.
Agreement between the reviewers was excellent for all evaluation factors (Table 4).
Intraclass correlation coefficients (ICCs) representing agreement between 2 reviewers for various evaluation factors pertaining to CT enterography in dogs.
| Evaluation factor | ICC |
|---|---|
| Attenuation measurement (HU) | |
| Portal vein | 0.89 |
| Mesenteric artery | 1.00 |
| Mesenteric vein | 0.99 |
| Duodenum | 0.96 |
| Jejunum | 0.84 |
| Ileum | 0.97 |
| Qualitative assessment | |
| Visualization of duodenum | 0.95 |
| Visualization of jejunum | 1.00 |
| Visualization of ileum | 0.83 |
| Visualization of peripheral vascularity | 0.80 |
| Image quality | 1.00 |
| Contrast-to-noise ratio | 0.94 |
Cutoffs for the ICC were as follows: < 0.40 = poor agreement, 0.41 to 0.6 = moderate agreement, 0.61 to 0.80 = good agreement, and < 0.80 = excellent agreement.
Discussion
All CT enterography techniques provided subjectively good-quality images for the assessment of the intestinal wall and mesenteric vessels in all dogs of the present study. The split technique simultaneously provided a homogeneously enhanced intestinal wall and markedly enhanced mesenteric vessels with a single CT scan. The total number of CT images required for interpretation could be reduced by half with the split technique and split-bolus tracking technique, compared with the dual-phase technique.
Images obtained by use of CT enterography with the split technique qualitatively provided enhancement of the intestinal wall similar to that for the dual-phase technique, except in the duodenum. However, enhancement of the intestinal wall of the duodenum and ileum was significantly less for the split-bolus tracking technique than for the dual-phase technique. Various enhancement patterns were observed for all 3 techniques. For the dual-phase technique, the mucosal layer was markedly enhanced in the arterial phase and then became homogeneous in the venous phase. We expected that the transmural pattern with high mucosal enhancement would be obtained with the split and split-bolus tracking techniques because the intestinal wall would be homogeneously enhanced after the first contrast agent injection and the mucosal layer would be enhanced after the second injection. However, for the split technique, transmural enhancement was observed in images of all dogs, similar to those of the venous phase of the dual-phase technique. Transmural enhancement with high mucosal attenuation was observed only in the arterial phase of the dual-phase technique.
The cranial mesenteric artery enters the serosa and supplies the muscular layer. Subsequently, blood flow continues into the submucosa and drains into the mucosal layer.17 In a study18 of intestinal blood perfusion in cats, rapid intense enhancement of the serosa and submucosa was observed by use of contrast-enhanced ultrasonography during the early phase after injection of the contrast agent, which was followed by gradual enhancement of the entire wall. In the late phase, the contrast agent was gradually washed out of the intestinal wall, with late persistence of submucosal enhancement. Mean arrival time of the contrast agent was 7.64 seconds, and time to peak enhancement after injection was 10.74 seconds.18 Although there were differences in the species and methods used between the study reported here and that study,18 CT images were acquired during the arterial phase of the dual-phase technique when iohexol reached the serosa, muscular layer, submucosa, and mucosa because the arterial scan delay was set at 7 seconds. For the split technique, CT images were obtained before the second injection of contrast agent would reach the mucosa; otherwise, mucosal enhancement would be too weak owing to the small dose of the second injection of contrast agent in the split technique.
Although the split technique could not provide an enhanced transmural wall with high mucosal enhancement, attenuation of the wall with the split technique was not significantly different from attenuation in the duodenum and jejunum for the dual-phase technique. The split technique can potentially be used to aid in the diagnosis of bowel ischemia; however, further research is required in veterinary medicine before clinical application. Moreover, attenuation of the enhanced ileal wall was significantly higher for the split technique than for the other 2 techniques. Considering that the ileum has a slightly thicker mucosal layer and slightly lower blood flow than does the jejunum, the second injection of contrast agent would enhance the mucosa of the ileum before the first injection of contrast agent completely exited the mucosal layer during the split technique.19 However, potential limitations with poorer visualization of the mucosa for the split technique, compared with visualization for the dual-phase technique, should be assessed in patients with intestinal diseases in future studies.
The duodenum receives blood from the celiac artery via the pancreaticoduodenal artery and from the cranial mesenteric artery via the caudal pancreaticoduodenal artery. The jejunum receives blood from the cranial mesenteric artery via the jejunal arteries. In the ileum, the mesenteric and antimesenteric sides are supplied from the ileocolic artery and cecal artery, respectively. The cranial mesenteric artery forms a complex arch-like structure (ie, arcade) within the mesentery that anastomoses with the jejunal and ileal arteries. Subsequently, the straight vascular branches (ie, vasa recta) course from the arterial arcades to the jejunum and ileum. The vasa recta in the jejunum are long and few, relative to those in the ileum, where they are short and numerous.
Visualization of the mesenteric vessels in the present study was evaluated on the basis of the extent of distribution of the enhanced vessels (eg, arcades and vasa recta) to the periphery of the intestinal serosa. Markedly enhanced mesenteric arteries and veins in the periphery were observed in the arterial and venous phases by use of the dual-phase technique and also by use of the split and split-bolus tracking techniques. Attenuation was significantly greater in the enhanced cranial mesenteric artery with the dual-phase technique than for both the split and split-bolus tracking techniques. However, the split techniques provided enhancement of the portal vein and mesenteric vein similar to that of the dual-phase technique, whereas enhancement was significantly lower with the split-bolus tracking technique. In addition, peripheral vascularity was more clearly visible at the level of the arterial arcade and vasa recta with the dual-phase technique than with the split and split-bolus tracking techniques; however, there was no significant difference. Because the peak of the contrast enhancement value depends on the dose of the contrast agent, the smaller dose of the second injection for the split technique may yield lower vascular enhancement than for dual-phase CT enterography.20 Therefore, a higher overall dose may be required for a split CT enterography technique to increase enhancement and visualization of the mesenteric vessels in the periphery.21 Although overall attenuation of the mesenteric vessels was less for the split technique than for the dual-phase technique, the serosal surface of the intestinal wall was more markedly visible with the split technique because of the hyperattenuated mesenteric arteries in the enhanced intestinal wall.
In the study reported here, a split CT enterography technique was performed by dividing the total dose of contrast agent into 2 injections (60% for the first injection and 40% for the second injection) on the basis of information in human medicine.16 Scan timing after IV injection of the contrast agent can be determined on the basis of the time-attenuation curve with the test bolus or bolus tracking techniques; administration of a test bolus of 0.5 mL/kg was followed by determination of the timing of the first and second injections of contrast agent. For the split technique, images were acquired when the venous scan delay and arterial scan delay matched. Bolus tracking can reduce the amount of time required for image acquisition because CT scanning is initiated when the number of HU in a region of interest reaches a threshold trigger point. Thus, for the bolus tracking technique, the timing of the second injection of contrast agent was determined by subtracting the scan delay for the arterial phase from the scan delay for the venous phase by use of data for the test bolus of the dual-phase technique; image acquisition then was initiated when the trigger point reached 100 HU. The split-bolus tracking technique provided enhancement similar to that of the split technique, but with significantly less enhancement of the portal vein, mesenteric artery, and mesenteric vein. This result may have been related to too low or high of a threshold for the trigger point, which was set at 100 HU on the basis of results for preliminary experiments.
Oral administration of contrast agent for CT enterography results in dilation of the intestinal lumen to enhance visual examination of the lumen and wall. In humans, 450 mL of dilute barium is orally administered 2 times at 30 and 45 minutes before CT image acquisition and 240 mL of water is administered immediately before the start of image acquisition.6 Dilute barium has the advantage of enabling excellent visual examination of all segments of the bowel, but it has some limitations for assessing mucosal discrimination of the intestine because of high attenuation.6 Water allows good visualization of the bowel with adequate luminal distension in the stomach; however, the distal portion of the small intestine is not distended sufficiently because of absorption in the proximal portion of the small intestine.6 Lactulose solution provides good intestinal distension, wall conspicuity, and contrast homogeneity. In a previous study2 involving CT enterography in dogs, a large volume (60 mL/kg) of dilute lactulose solution was administered to anesthetized dogs continuously over a 45-minute period to maximize dilation of the lumen in all small intestinal segments. In the present study, we also used dilute lactulose solution as an orally administered agent; however, we administered half of the total dose (30 mL/kg for each dose with a 20-minute interval between doses). In addition, butylscopolamine bromide, an anticholinergic agent, was used to modulate gastrointestinal motility to induce relaxation of the intestinal smooth muscle and stagnation of bowel luminal contents.22,23
The present study had some limitations. First, only a small number of healthy dogs were used, and patients with enteric diseases were not included. Additional studies of the split CT enterography techniques in a large population of dogs are needed to confirm results of this study. Second, the timing for injection of the contrast agent in the split-bolus tracking technique was determined on the basis of results for the test bolus of the dual-phase technique. Thus, there could have been a difference between the test bolus results and the time when the arterial and venous phases were initiated during the split technique because the dose of the contrast agent differed. Third, the threshold of the trigger point for the split-bolus tracking technique was set at 100 HU on the basis of preliminary experiments with a limited number of dogs. Despite these limitations, both split techniques provided good CT enterography images for evaluation of the intestine and mesenteric vessels, similar to images obtained with the dual-phase technique.
In the study reported here, split techniques for CT enterography were assessed by comparing those results with results for the dual-phase technique and also by comparing results for the split technique with those for the split-bolus tracking technique. Images obtained with CT enterography by use of the split technique had sufficient enhancement of the intestinal wall, which was similar to results for the dual-phase technique. The split technique also resulted in enhancement of the mesenteric vessels of the peripheral region with good conspicuity, similar to results for the dual-phase technique. A split technique for CT enterography can decrease the scan time, radiation exposure, and the number of CT images required for interpretation, compared with dual-phase CT enterography. Results this study indicated that CT enterography with a split-bolus technique was feasible for evaluation of the intestinal wall and mesenteric vessels of healthy dogs and provided images that were of quality similar to images obtained with the dual-phase technique. Use of a split-bolus technique could reduce the number of CT images required for interpretation and reduce the time required for acquisition of images.
Acknowledgments
Supported by the Animal Medical Institute of Chonnam National University and the Basic Science Research Program through the National Research Foundation of Korea funded by the Ministry of Science, ICT, and Future Planning (grant No. NRF-2018R1A2B6006775).
The authors declare that there were no conflicts of interest.
Footnotes
Colyte, Taejoon Pharmaceutical Co, Seoul, Republic of Korea.
Alfaxane, Jurox Pty Ltd, Rutherford, NSW, Australia.
Terrell, Piramal Critical Care, Bethlehem, Pa.
Buscopan, Labiana Life Sciences, Barcelona, Spain.
Siemens Emotion 16, Siemens, Forchheim, Germany.
Omnipaque 300, GE Healthcare, Oslo, Norway.
Medrad Vistron CT injection system, Medrad Inc, Warrendale, Pa.
CARE Bolus, Siemens Medical Systems, Berlin, Germany.
Infinitt PACS, Infinitt Healthcare Co, Seoul, Republic of Korea.
IBM SPSS statistics, version 21, IBM Corp, Armonk, NY.
References
1. Gourtsoyianni S, Zamboni GA, Romero JY, et al. Routine use of modified CT enterography in patients with acute abdominal pain. Eur J Radiol 2009;69:388–392.
2. Keh S, Sohn J, Choi M, et al. Evaluation of computed tomographic enterography with an orally administered lactulose solution in clinically normal dogs. Am J Vet Res 2016;77:367–373.
3. Elsayes KM, Al-Hawary MM, Jagdish J, et al. CT enterography: principles, trends, and interpretation of findings. Radiographics 2010;30:1955–1970.
4. 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;26:641–662.
5. Arslan H, Etlik O, Kayan M, et al. Peroral CT enterography with lactulose solution: preliminary observations. Am J Roentgenol 2005;185:1173–1179.
6. 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 Med 2010;2:186–191.
7. Raptopoulos V, Davis MA, Smith EH. Imaging of the bowel wall. Computed tomography and fat density oral-contrast agent in an animal model. Invest Radiol 1986;21:847–850.
8. Terragni R, Vignoli M, Rossi F, et al. Stomach wall evaluation using helical hydro-computed tomography. Vet Radiol Ultrasound 2012;53:402–405.
9. Hoey S, Drees R, Hetzel S. Evaluation of the gastrointestinal tract in dogs using computed tomography. Vet Radiol Ultrasound 2013;54:25–30.
10. 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.
11. Huprich JE, Barlow JM, Hansel SL, et al. Multiphase CT enterography evaluation of small-bowel vascular lesions. AJR Am J Roentgenol 2013;201:65–72.
12. Chow LC, Kwan SW, Olcott EW, et al. Split-bolus MDCT urography with synchronous nephrographic and excretory phase enhancement. AJR Am J Roentgenol 2007;189:314–322.
13. Scialpi M, Pierotti L, Gravante S, et al. Split-bolus versus triphasic multidetector-row computed tomography technique in the diagnosis of hepatic focal nodular hyperplasia: case report. J Med Case Rep 2014;8:425–430.
14. Leung VJ, Grima M, Khan N, et al. Early experience with a split-bolus single-pass CT protocol in paediatric trauma. Clin Radiol 2017;72:497–501.
15. Biscaldi E, Ferrero S, Remorgida V, et al. MDCT enteroclysis urography with split-bolus technique provides information on ureteral involvement in patients with suspected bowel endometriosis. AJR Am J Roentgenol 2011;196:W635–W640.
16. Boos J, Fang J, Chingkoe CM, et al. Split-bolus injection producing simultaneous late arterial and portal venous phases in CT enterography: preliminary results. AJR Am J Roentgenol 2017;209:1056–1063.
17. Granger DN, Richardson PD, Kvietys PR, et al. Intestinal blood flow. Gastroenterology 1980;78:837–863.
18. Diana A, Specchi S, Toaldo MB, et al. Contrast-enhanced ultrasonography of the small bowel in healthy cats. Vet Radiol Ultrasound 2011;52:555–559.
19. Hulten L, Jodal M, Lindhagen J, et al. Blood flow in the small intestine of cat and man as analyzed by an inert gas washout technique. Gastroenterology 1976;70:45–51.
20. Dean PB, Violante MR, Mahoney JA. Hepatic CT contrast enhancement: effect of dose, duration of infusion, and time elapsed following infusion. Invest Radiol 1980;15:158–161.
21. Valle C, Bonaffini PA, Barletta A, et al. Split-bolus MDCT urography technique: clinical applications, imaging findings and radiation dose exposure. Eur J Radiol 2017;1618:1–23.
22. Sagrada A, Schiavone A, Cefala 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.
23. Sun Y, Song G, Yin J, et al. Effects and mechanisms of electroacupuncture on glucagon-induced small intestinal hypomotility in dogs. Neurogastroenterol Motil 2010;22:1217–1223.
Appendix
Parameters for performance of CT enterography in dogs by use of 3 techniques.
| Variable | Dual phase | Split | Split-bolus tracking |
|---|---|---|---|
| No. of contrast CT scans | 3 | 2 | 1 |
| Test bolus | Injected | Injected | Not injected |
| Iohexol dose (mg of 1/kg) | |||
| Total | 2.5 | 2.5 | 2.5 |
| Test bolus | 0.5 | 0.5 | — |
| Postcontrast scan | 2.0 | 2.0 | 2.5 |
| Ratio of split contrast agent doses | — | 60:40 | 60:40 |
| Initiation of CT scan | Based on arterial scan delay and venous scan delay | When arterial scan delay and venous scan delay matched | When trigger point reached 100 HU |
— = Not applicable.
Appendix 2
Scoring system used for qualitative evaluation of CT enterography in dogs.
| Factor | Description | Score |
|---|---|---|
| Visibility of peripheral vascularity | Only arcade vascularity visible; vasa recta vascularity not visible | 1 |
| Arcade and vasa recta vascularity somewhat visible, compared with in the intestine | 2 | |
| Arcade and vasa recta vascularity markedly visible, compared with in the intestine | 3 | |
| Enhancement of intestinal wall | Enhancement of artery only; no enhancement of intestinal wall | 1 |
| Enhancement of mucosal layer only | 2 | |
| Transmural enhancement including entire intestinal wall | 3 | |
| Transmural enhancement with marked mucosal enhancement | 4 | |
| Image quality | CT images difficult to interpret because of artifacts | 1 |
| Moderately good CT images with some artifacts | 2 | |
| Optimal CT images with few or no artifacts | 3 |
The arcade represented an arch-like structure of the cranial mesenteric artery created by a series of anastomosing arterial branches in the mesentery, and the vasa recta represented straight arteries arising from the arcades.
