Radiography and ultrasonography are the most important imaging modalities to evaluate the small intestine of veterinary patients because they are noninvasive and inexpensive and often can be performed without sedation or anesthesia.1–4 Abnormalities of the small intestine, including perforation (especially without pneumoperitoneum), obstruction, and abnormal motility, may be difficult to identify with conventional radiography and ultrasonography. Therefore, radiographic and ultrasonographic contrast studies may be helpful to identify these small intestinal abnormalities.2–5
In veterinary medicine, barium sulfate is the most commonly used positive-contrast medium for radiographic study of the gastrointestinal tract, partly because it is cost-effective.2,3,6 However, the study can take approximately 3 to 5 hours2,3 to complete and be nondiagnostic when barium flocculation occurs.5,6 Additionally, barium in the lungs and abdominal cavity, because of esophageal and intestinal perforation or devitalization, causes severe inflammation.2,7–9 Barium administration is contraindicated for people and dogs with a high risk of pulmonary aspiration because of vomiting or high suspicion of gastrointestinal tract perforation and when other procedures (eg, esophagogastroduodenoscopy, abdominal ultrasonography, or abdominal surgery) are to immediately follow contrast radiography. Rather, an iodinated contrast medium may be a better choice of contrast agent in these situations; also, iodinated contrast radiographic studies can take only 1 to 2 hours to complete.2,3,6–9
Iodinated contrast medium can be ionic or nonionic. Ionic iodinated contrast medium is contraindicated in puppies, kittens, and dehydrated patients because of its hyperosmolarity.8,10,11 After its oral administration, fluid movement from the blood vessels into the lumen of the gastrointestinal tract may cause hypovolemic shock; after pulmonary aspiration of ionic iodinated contrast medium, fluid may move into the alveoli, causing pulmonary edema.8,10,11 Alternatively, nonionic iodinated contrast medium is considered safer because it has lower osmolarity and, therefore, is not expected to cause hypovolemic shock.8,10–12 Yet, nonionic iodinated contrast medium has a high cost, low viscosity, and reduced contrast effect over time.2,3,13 Because this medium has low viscosity, the gastrointestinal tract mucosa can be difficult to evaluate, and because of absorption and dilution of the medium as time elapses after its administration, its contrast effect decreases.
Carboxymethylcellulose is a nontoxic, nonimmune, biodegradable, and bioabsorbable substance that is used in cosmetics and medicines and as a food additive. As a radiographic contrast medium, it is useful because of its low risk of causing adverse events, especially when it is aspirated into the lungs and leaks into the abdominal cavity.14–23 Also, CMC is not absorbed by the small intestine and is viscous, unlike nonionic iodinated contrast medium; therefore, visualization of the small intestinal mucosa and lumen is improved because CMC coats the mucosa and its contrast effect is not diluted. In people and dogs, CMC has been administered with barium to prevent barium flocculation and shorten radiographic study time.1,13,20,21
Small intestinal motility and wall structure (eg, thickness and layering) can be assessed with ultrasonography. However, accurate small intestinal ultrasonography requires an experienced sonographer and sufficient time because the structure of the small intestine is complex and small intestinal walls are frequently obscured by intraluminal gas.2–4,7 Ideally, ultrasonography should precede barium contrast radiography because barium absorbs ultrasonic waves, thereby reducing ultrasonographic image quality.3,24
Ultrasonography after oral administration of polyethylene glycol solution to people with celiac or Crohn disease reveals that this solution adequately distended the small intestinal lumen and improved visualization of the small intestinal walls.4,23 Ultrasonography after administration of polyethylene glycol to people with Crohn disease is also as useful as abdominal contrast (barium) radiography to detect small intestinal lesions.23 Therefore, oral administration of a contrast medium, other than barium, to dogs may also be helpful for detecting small intestinal lesions ultrasonographically.
The goal of the study reported here was to evaluate MCMs that combined the respective advantages and offset the respective disadvantages of a nonionic iodinated contrast medium and CMC such that the MCM can be used to optimally evaluate the small intestine of dogs radiographically and ultrasonographically, especially when contrast radiography precedes ultrasonography. We hypothesized that the MCM with the largest volume of iohexol per kilogram of a dog's body weight would provide the best small intestinal radiographic images. Also, we believed each MCM would facilitate ultrasonographic assessment of the small intestine.
Materials and Methods
Animals
Eight adult Beagles (7 sexually intact males and 1 sexually intact female) with a mean age of 31 months (SD, 12.8 months; range, 18 to 60 months) from a research colony were included in the study. Mean body weight was 12.4 kg (SD, 1.3 kg; range 10.2 to 14.1 kg) and body condition score (scale, 1 to 9) was 5.5 (SD, 0.9; range, 4 to 7). All dogs were considered healthy on the basis of physical examination and results of CBC and serum biochemical analyses. Dogs were individually housed indoors in cages and were assessed daily during the entire study. Food was withheld for at least 12 hours before the procedures, but dogs had access to water at all times. The study was approved by the Institutional Animal Care and Use Committee of Seoul National University (protocol No. SNU-190705-1).
Procedures
Radiography and ultrasonography—After dogs were fasted for 12 hours, survey abdominal radiographya (70 kVp, 300 mA, and exposure time of 0.015 seconds) was performed to confirm that the gastric lumen did not contain ingesta. If ingesta was seen, the study was postponed to another day. With a 4- to 10-MHz convex transducer and a 5- to 13-MHz linear transducer, ultrasonographyb was performed to confirm that the small intestine could be adequately assessed and no abnormalities were seen. Dogs were positioned without sedation in right lateral and dorsal recumbency for radiography and in dorsal recumbency for ultrasonography. Ultrasonography was performed by one of the authors (JK).
Contrast medium was administered through an orogastric tube, and serial abdominal radiographs (right lateral and ventrodorsal views) and ultrasonographic images of the duodenum, jejunum, and ileum were obtained every 10 minutes until the contrast medium reached the proximal portion of the ascending colon.
Contrast medium—A 0.5% CMC solution was made by dissolving CMC powderc in sterile water that was heated to 60°C to 70°C on a hot plate and stirred with a magnetic stirrer.d Then, MCM was made by combining 0.5% CMC solution and iohexol (300 mg of I/mL),e with a volume of iohexol equal to 0.5, 1.0, or 1.5 mL of iohexol/kg of body weight. The total volume of MCM administered was 10 mL/kg, such that the first MCM combined 9.5 mL of CMC/kg and 0.5 mL of iohexol/kg; the second, 9 mL/kg and 1 mL/kg; and the third, 8.5 mL/kg and 1.5 mL/kg, respectively. Radiography and ultrasonography were repeated 2 times/dog, with at least a 1-week washout period between treatments. Dogs were not randomized for treatment order; all dogs received the first MCM first, the second MCM second, and the third MCM third.
Image analysis—A total of 24 radiographic and ultrasonographic image sets (3/dog) were obtained and evaluated by 4 radiologists (JK, DO, JC, and KK) through a picture-archiving and communication system.f Image sets were anonymized and reviewed at the end of the study, and radiologists were blinded to the MCM administered.
Radiograph quality was judged on the degree of small intestinal contrast enhancement, compared with bone; clarity of a contrast-enhanced segment of small intestine when superimposed by ≥ 1 contrast-enhanced small intestinal segment or by bone; and visualization of the ileocolic junction and cecum. Radiologists independently scored each criterion using a 5-point scale, with 4 = excellent, 3 = very good, 2 = good, 1 = fair, and 0 = poor (Appendices 1–4). Gastric emptying time (time from administration of MCM to time when the gastric lumen was devoid of MCM), gastrointestinal transit time (time from administration of MCM to time when MCM was within the lumen of the proximal ascending colon), and the final times when the contrast-enhanced duodenum, jejunum, and ileum could be radiographically evaluated (final observation time) were recorded. The width for each maximally distended (with MCM) small intestinal segment (duodenum, jejunum, and ileum) was measured 3 times and the average measurement recorded. For small intestinal lumens maximally distended with MCM and gas such that the intestinal walls could be seen (ie, double-contrast effect), wall thicknesses were similarly measured and recorded as a single combined value. Because of variability in luminal distension and peristalsis, the thickness of each wall for each maximally distended segment could vary. However, because wall thicknesses were assumed to be symmetric (ie, wall thickness of one wall was the same for the opposite wall for the maximally distended segment), unilateral wall thickness was determined by dividing the reported single value by 2.
Ultrasonographically, the number of dogs with an open ileocolic valve, determined by witnessing movement of MCM from the terminal portion of the ileum to the proximal portion of the ascending colon, was recorded.
Statistical analysis
To identify interobserver reliability, intraclass correlation coefficients were calculated. A correlation coefficient < 0.59 was considered poor, between 0.60 and 0.79 fair, and between 0.80 and 1.00 excellent. The Kruskal-Wallis test was used to determine whether any differences in radiographic image quality scores existed among the 3 treatments, and the Mann-Whitney U test was used to separately determine whether any differences existed between pairs of the 3 treatments (3 pairwise comparisons). Commercial statistical softwareg was used for the analyses. Values of P < 0.05 were considered significant.
Results
Throughout the study, all dogs remained in good condition and ate well, and no weight loss, diarrhea, or vomiting was observed.
Intraclass correlation coefficients among the 4 radiologists’ scores for each criterion of radiographic image quality were > 0.8. The MCM that combined 8.5 mL of CMC/kg and 1.5 mL of iohexol/kg yielded the highest radiographic image quality scores for each criterion and the highest total score (P < 0.01; Table 1; Figure 1). Mean ± SD gastric emptying time was 73.23 ± 22.39 minutes and mean ± SD gastrointestinal transit time was 86.46 ± 24.13 minutes. The final times when MCM was observed within the lumens of the duodenum, jejunum, and ileum were summarized. Mean ± SD maximum diameter of the small intestine was 14.05 ± 0.20 mm (Figure 2), and thickness of the duodenal, jejunal, and ileal walls was approximately 1 mm (Table 2). The ileocolic junction was seen after administration of all MCMs (Figure 3).
Ventrodorsal radiographic views of the abdomen obtained after oral administration of 1 of 3 MCMs to 8 healthy adult Beagles to assess each MCM's ability to enhance the small intestine. A—Obtained 90 minutes after administration of an MCM that combined 9.5 mL of 0.5% CMC/kg and 0.5 mL of iohexol/kg. B—Obtained 60 minutes after administration of an MCM that combined 9 mL of 0.5% CMC/kg and 1 mL of iohexol/kg. C—Obtained 40 minutes after administration of an MCM that combined 8.5 mL of 0.5% CMC/kg and 1.5 mL of iohexol/kg.
Citation: American Journal of Veterinary Research 81, 12; 10.2460/ajvr.81.12.950
Ventrodorsal radiographic views of the abdomen from the dogs of Figure 1 after oral administration of an MCM that combined 8.5 mL of 0.5% CMC/kg and 1.5 mL of iohexol/kg. Note the variable but increasing amounts of small intestinal intraluminal gas (A < B < C < D), with the most gas and, therefore, the best visualization of the small intestinal walls, in D.
Citation: American Journal of Veterinary Research 81, 12; 10.2460/ajvr.81.12.950
Ventrodorsal radiographic views of the abdomen from the dogs of Figure 1 after oral administration of an MCM that combined 9.5 mL of 0.5% CMC/kg and 0.5 mL of iohexol/kg (A), 9 mL of 0.5% CMC/kg and 1 mL of iohexol/kg (B), and 8.5 mL of 0.5% CMC/kg and 1.5 mL of iohexol/kg (C). Note the ileocolic junction (arrow).
Citation: American Journal of Veterinary Research 81, 12; 10.2460/ajvr.81.12.950
Scores (range, 0 [poor] to 4 [excellent]) assigned on the basis of 4 criteria for assessing the radiographic appearance of the small intestine after independent review by 4 radiologists of abdominal radiographs obtained starting 10 minutes after oral administration of MCMs that differed by the volume of iohexol to 8 healthy adult Beagles.
| Criterion | MCM* | Mean ± SD score |
|---|---|---|
| Degree of contrast enhancement | 0.5 mL/kg | 2.4 ± 0.5 |
| 1.0 mL/kg | 3.6 ± 0.5 | |
| 1.5 mL/kg | 4.0 ± 0.0† | |
| Clarity, with superimposed small intestine | 0.5 mL/kg | 2.1 ± 0.4 |
| 1.0 mL/kg | 3.4 ± 0.7 | |
| 1.5 mL/kg | 4.0 ± 0.0† | |
| Clarity, with superimposed bone | 0.5 mL/kg | 1.4 ± 0.7 |
| 1.0 mL/kg | 3.1 ± 0.8 | |
| 1.5 mL/kg | 3.8 ± 0.5† | |
| Visualization of terminal ileum | 0.5 mL/kg | 2.1 ± 1.3 |
| 1.0 mL/kg | 3.3 ± 0.9 | |
| 1.5 mL/kg | 4.0 ± 0.0† | |
| Total | 0.5 mL/kg | 8.0 ± 2.0 |
| 1.0 mL/kg | 13.4 ± 2.0† | |
| 1.5 mL/kg† | 15.8 ± 0.5† |
Indicates the millimeters of iohexol per kilogram of body weight (dose) administered to each dog. Each MCM was created by a combination of 0.5% CMC and iohexol (300 mg of I/mL). The dose of MCM was 10 mL/kg, regardless of the dose of iohexol (ie, 0.5 mL of iohexol/kg plus 9.5 mL of CMC/kg equaled 10 mL of MCM/kg).
Score significantly greater (P < 0.01), compared with 0.5 mL/kg.
Radiographic variables for small intestinal segments obtained after administration of MCMs to the dogs of Table 1.
| Small intestinal segment | |||
|---|---|---|---|
| Radiographic variable | Duodenum | Jejunum | Ileum |
| Final observation time* (min) | 51.88 ± 21.41 | 74.79 ± 20.46 | 92.08 ± 23.63 |
| Maximum diameter† (mm) | 14.17 ± 3.17 | 13.82 ± 1.89 | 14.15 ± 2.28 |
| Combined wall thickness‡ (mm) | 1.98 ± 0.33 | 2.11 ± 0.38 | 1.93 ± 0.38 |
| Unilateral wall thickness§ (mm) | 0.99 ± 0.16 | 1.06 ± 0.19 | 0.97 ± 0.19 |
Results are expressed as mean ± SD.
Final time when MCM could be seen in each small intestinal segment (duodenum, jejunum, and ileum).
The width of each maximally distended (with MCM) segment was measured 3 times/radiologist, and the average for each radiologist was recorded.
For small intestinal lumens maximally distended with MCM and gas such that the intestinal walls could be seen (ie, double-contrast effect), wall thicknesses were similarly measured and recorded as a single, combined value (ie, for maximally distended double-contrast segment, total width of segment – width of lumen = combined thickness of walls).
Because wall thicknesses of a single maximally distended double-contrast segment were assumed to be symmetric, unilateral wall thickness was determined by dividing the single measurement by 2.
Ultrasonography revealed that all 3 MCMs could be used to evaluate the small intestinal walls without artifact or interference with the evaluation of other abdominal structures. Minimal reverberation artifact was seen because of intraluminal gas, but walls were clearly seen (Figure 4). The MCM appeared anechoic, but as the number of gas bubbles increased with peristalsis, the MCM appeared echogenic (Figure 5). In 17 of 24 (70.8%) image sets, the ileocolic valve opening was clearly identified, and the MCM was seen to move from the terminal portion of the ileum to the proximal portion of the ascending colon (Figure 6).
Ultrasonographic images of a portion of the small intestine of a dog of Figure 1. Intraluminal gas and associated reverberation artifact moved with normal peristalsis from the left (A and B) to the right (C) and then beyond the transducer's plane of view (D). Note that the near and far fields of the small intestinal walls are clearly seen.
Citation: American Journal of Veterinary Research 81, 12; 10.2460/ajvr.81.12.950
Ultrasonographic images of the walls and lumen of a portion of small intestine from a dog of Figure 1. A—The MCM appears anechoic within the lumen. B—With the presence of gas bubbles within the lumen, MCM appears echogenic.
Citation: American Journal of Veterinary Research 81, 12; 10.2460/ajvr.81.12.950
Ultrasonographic images of the ileocolic junction (arrow) from the dogs of Figure 1. A—Accumulated MCM in the terminal portion of the ileum (I). B—When a threshold volume of MCM was achieved, MCM moved from the terminal portion of the ileum through an open ileocolic valve to the proximal portion of the ascending colon (C).
Citation: American Journal of Veterinary Research 81, 12; 10.2460/ajvr.81.12.950
Discussion
The objective of the study reported here was to evaluate MCM that combined nonionic iodinated contrast medium (iohexol) and CMC for radiography and ultrasonography of the small intestine of healthy dogs. Results indicated that an MCM that combined 8.5 mL of 0.5% CMC/kg and 1.5 mL of iohexol/kg was optimal for radiographic evaluation.
Radiographically, MCM sufficiently distended the small intestinal lumen. Contrast enhancement did not lessen as time elapsed, which suggested that MCM was not subject to absorption and dilution; therefore, good image quality remained. In addition, when small intestinal segments were superimposed with other small intestinal segments, MCM with iohexol doses of 1 mL/kg or 1.5 mL/kg still permitted their adequate assessment (ie, superimposed segments could be distinguished and sufficiently evaluated). Concurrent gas within the intestinal lumen also allowed for the intestinal mucosa to be seen (double-contrast effect). Gas (air) may have been introduced with administration of MCM through the orogastric tube or with normal respiration before or during the study. Gastrointestinal transit time for all MCMs was approximately 90 minutes, faster than that reported with barium (3 to 5 hours) and similar to that reported with iohexol alone.2,3,8
Radiography also revealed small intestinal wall thickness to be approximately 1 mm. In dogs, however, wall thickness determined from radiographs has not been reported but is reported2,3 to be 3 to 5 mm on the basis of ultrasonography, likely because of variable luminal distention at the time of measurement. Ultrasonographically, a 2-mm difference is reported25 for the wall thicknesses of human small intestine when its lumen is distended (3 mm) versus nondistended (5 mm). Therefore, wall thickness of 1 mm was considered to be normal for the dogs in the present study because of luminal distention by MCM.2,3,25
Additionally, ultrasonographically, the presence of MCM enabled identification of the far-field wall, which sometimes may be difficult to see because of reverberation artifact caused by intraluminal gas, and did not interfere with visualization of the surrounding structures, regardless of the MCM combination and its echogenicity. The MCM became echogenic when the amount of gas bubbles increased during rapid peristalsis and anechoic as peristalsis decreased.
The ileocolic junction was well identified radiographically and ultrasonographically. Modified contrast medium accumulated at the terminal portion of the ileum and was observed to move into the proximal portion of the ascending colon.
The optimal MCM combined CMC with 1.5 mL of iohexol/kg, which was 50% to 75% of the recommended dose (2 to 3 mL/kg) of iohexol (300 mg of iodine/mL) used alone for radiographic contrast enhancement of the small intestine in dogs and cats.2,3,8,10,26 Cost of contrast media varies, and iohexol is approximately 60 times as expensive/mL as barium at our institution. For a 10-kg dog, the cost is 18 times as much. However, MCM used in the present study was economical at our institution, with a cost of only 9 times that of barium and 50% less expensive than iohexol. Although the cost differences at our institution may not be as great as at other institutions, cost of this MCM is suspected to be less than iohexol.
The present study had several limitations. Only a small number of dogs were included, and those dogs were healthy Beagles; optimal MCM for the assessment of other breeds is unknown. Plus, imaging studies of the small intestine after administration of barium and iohexol alone to those Beagles were not performed, such that comparisons among contrast media could not be determined. Lastly, MCM's applicability to dogs with various small intestinal diseases is unknown.
In conclusion, administration of 10 mL of MCM/kg, a combination of 8.5 mL of 0.5% CMC/kg and 1.5 mL of iohexol/kg, yielded optimal radiographic and ultrasonographic image quality for assessment of the small intestine of healthy Beagles. Radiographic contrast enhancement was adequate even when small intestinal segments were superimposed with bone and other contrast-enhanced small intestinal segments. Ultrasonographically, MCM allowed for good evaluation of the small intestinal walls by mitigating reverberation artifact, secondary to intraluminal gas. In addition, MCM permitted contrast radiography to be performed immediately prior to abdominal ultrasonography without interfering with the latter. Therefore, MCM has potential as a dual-purpose contrast medium for the assessment of the small intestine in dogs.
Acknowledgments
The study was supported in part by the Research Institute for Veterinary Science at Seoul National University.
The authors declare that there were no conflicts of interest.
ABBREVIATIONS
| CMC | Carboxymethylcellulose |
| MCM | Modified contrast medium |
Footnotes
EVA-HF525 machine, GEMSS, Gyeonggi-do, Republic of Korea.
ProSound Alpha 7, Hitachi-Aloka, Tokyo, Japan.
Carboxymethylcellulose sodium salt, Sigma Chemical Co, St Louis, Mo and Kukjeon Pharm, Seoul, Republic of Korea.
Magnetic stirrer, MS 300, BANTE, Shanghai, China.
Omnipaque 300, GE Healthcare, Cork, Ireland.
Vet PACS, Infinitt Healthcare Co Ltd, Seoul, Republic of Korea.
SPSS Statistics for Windows, version 23.0, IBM Corp, Armonk, NY.
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Appendix 1
Scoring system for assessing the degree of radiographic small intestinal contrast enhancement.
| Score | Description |
|---|---|
| Excellent (4) | Small intestinal segment with greater contrast enhancement vs bone; no superimposition with other structures. |
| Very good (3) | Small intestinal segment with equal contrast enhancement vs bone; no superimposition with other structures. |
| Good (2) | Small intestinal segment with less contrast enhancement vs bone; no superimposition with other structures. |
| Fair (1) | Small intestinal segment with less contrast enhancement vs bone and unclear margin; no superimposition with other structures. |
| Poor (0) | Small intestinal segment with little contrast enhancement; no superimposition with other structures. |
Appendix 2
Scoring system for assessing the radiographic clarity of a contrast-enhanced small intestinal segment when superimposed by ≥ 1 contrast-enhanced small intestinal segment.
| Score | Description |
|---|---|
| Excellent (4) | Superimposition of ≥ 2 contrast-enhanced small intestinal segments that were distinguishable by ≥ 80%; no superimposed bone. |
| Very good (3) | Superimposition of ≥ 2 contrast-enhanced small intestinal segments that were distinguishable by ≥ 60% and < 80%; no superimposed bone. |
| Good (2) | Superimposition of ≥ 2 contrast-enhanced small intestinal segments that were distinguishable by ≥ 40% and < 60%; no superimposed bone. |
| Fair (1) | Superimposition of ≥ 2 contrast-enhanced small intestinal segments that were distinguishable by ≥ 20% and < 40%; no superimposed bone. |
| Poor (0) | Superimposition of ≥ 2 contrast-enhanced small intestinal segments that were distinguishable by < 20%; no superimposed bone. |
Appendix 3
Scoring system for assessing the radiographic clarity of a contrast-enhanced small intestinal segment when superimposed with bone.
| Score | Description |
|---|---|
| Excellent (4) | Contrast-enhanced small intestinal segment distinguishable by ≥ 80% from superimposed bone. |
| Very good (3) | Contrast-enhanced small intestinal segment distinguishable by ≥ 60% and < 80% from superimposed bone. |
| Good (2) | Contrast-enhanced small intestinal segment distinguishable by ≥ 40% and < 60% from superimposed bone. |
| Fair (1) | Contrast-enhanced small intestinal segment distinguishable by ≥ 20% and < 40% from superimposed bone. |
| Poor (0) | Contrast-enhanced small intestinal segment distinguishable by < 20% from superimposed bone. |
Appendix 4
Scoring system for assessing the radiographic appearance of the ileocolic junction and cecum.
| Score | Description |
|---|---|
| Excellent (4) | Marked contrast enhancement of the ileocolic junction and cecum. |
| Very good (3) | Moderate contrast enhancement of the ileocolic junction and cecum. |
| Good (2) | Moderate contrast enhancement of either (not both) the ileocolic junction or cecum. |
| Fair (1) | Mild contrast enhancement of either (not both) the ileocolic junction or cecum. |
| Poor (0) | No contrast enhancement of the ileocolic junction and cecum. |
