Cerebrovascular accidents (CVAs), commonly known as stroke in humans, result from pathological changes in supplying blood vessels into the brain.1 Although the incidence of CVAs in dogs has not been accurately reported, it is estimated to be approximately 2%.1 However, CVA is becoming increasingly detected with the development of advanced diagnostic techniques; therefore, it is speculated that the actual prevalence is higher than previously reported.2 CVAs are primarily divided into ischemic and hemorrhagic strokes, with ischemic stroke being more common in small animals.3 Ischemic stroke in dogs is mainly caused by vascular obstructions such as thrombosis and embolism in blood vessels. In veterinary medicine, the most common artery that develops emboli is the rostral cerebellar artery, and the regions known to be sensitive to ischemic stroke are the cerebellum, hippocampus, parietal lobe, and occipital lobe.2,4 The occurrence of neurologic deficits due to ischemic stroke varies depending on the location of the stroke and generally present as acute onset that lasts for at least 24 hours.1,2
Various diagnostic techniques such as magnetic resonance angiography, diffusion-weighted magnetic resonance imaging (MRI), perfusion-weighted MRI (PWMRI), and perfusion computed tomography (PCT) have been developed for the diagnosis of stroke in human medicine. Particularly, both PWMRI and PCT are useful for the early diagnosis of CVAs by detecting hemodynamic changes.2 By providing information about tissue viability, both methods allow identification of the extent of the affected tissue and differentiate between an infarction core that is an irreversibly hypoperfused area and that is a penumbra, which is still a viable tissue surrounding the infarction core.2,5
In general, MRI is widely used to diagnose neurologic diseases; however, PCT is more useful in patients with a high risk of anesthesia owing to its shorter scanning time than PWMRI.2 PCT also has high diagnostic value with high sensitivity and specificity for ischemia in both animals and humans.6,7 Another advantage of PCT over PWMRI is the ease of quantitatively analyzing perfusion measurements.8 This allows the use of PCT parameter values as thresholds for cerebrovascular diseases. In addition, it is easy to perform and is cost-effective because of the wider accessibility of CT than MRI.7
PCT evaluates blood flow after a single injection of a conventional contrast medium and provides hemodynamic information using various perfusion parameters.2,8 As contrast medium flows into cerebral arteries and veins, the change in pixel enhancement in these vessels (measured in HU) is presented as time-density curve (TDC) graphs.7 Perfusion mapping can then be derived based on TDC graphs, providing visual information about perfusion deficits in the ischemic area.9
The perfusion parameters that can be obtained by mapping include cerebral blood volume (CBV), cerebral blood flow (CBF), time to peak of tissue enhancement (TTP), mean transit time (MTT), and time-to-maximum of the residual function (Tmax), all of which indirectly reflect hemodynamic changes in blood flow.
There have been many studies on the factors influencing the results of brain perfusion imaging in human medicine.10–12 Among several variables, the contrast medium injection rate and intravenous catheter size are considered major factors influencing perfusion scanning.13 These studies have been used as the basis for establishing a standardized scanning protocol for brain PCT in human medicine.14,15
In veterinary medicine, PCT has been used in disease diagnoses that require perfusion evaluation. Several studies on variables affecting PCT have been conducted in abdominal organs such as the liver,16 kidney,17,18, and pancreas.19 In addition, studies on the diagnosis of cerebrovascular diseases that require perfusion evaluation, such as degenerative diseases20 and brain tumors21 have been performed. However, studies on the variables influencing brain PCT have not been conducted.
Thus, the objective of this study was to evaluate the effect of different contrast medium injection rates and intravenous catheter sizes on TDC of brain PCT in clinically normal Beagles and provide a reference range for the perfusion parameters of the areas of the brain sensitive to ischemic changes for clinical application of PCT as a potential diagnostic method for ischemic cerebrovascular disease in small animals.
Materials and Methods
Animal preparation
Five healthy, sexually intact male Beagles without evidence of central nervous system dysfunction were used in this experimental study. Before the study, the health status of each dog was evaluated through physical examination, neurologic examination, CBC, serum biochemical analyses, radiography, abdominal ultrasonography, and echocardiography. This study was approved by the Institutional Animal Care and Use Committee of Konkuk University (Approval No. KU22187). All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.
Brain PCT
Protocols for experiments and anesthesia—This study was designed as a cross-over study and conducted for 2 months (from February 28, 2022, to April 26, 2022). In all dogs, brain PCT was performed 6 times under 2 conditions: (1) different injection rates (2, 3, and 4 mL/second) of contrast medium and (2) different intravenous (IV) catheter sizes (24-gauge and 20-gauge). The first examination was conducted using a 24-gauge catheter with 3 different injection rates, and the same procedure was repeated using a 20-gauge catheter 2 weeks later. All the IV catheters were placed in the left cephalic vein. A contrast medium was directly administered to the catheter hub.
Before anesthesia, the dogs were fasted for at least 12 hours. The heart rate and mean blood pressure were examined every 5 minutes during the anesthesia procedures. Propofol (6 to 8 mg/kg, IV) was used in the induction process and endotracheal intubation was performed. General anesthesia was maintained with 2.0% isoflurane inhalation. Anesthetic depth was controlled to minimize the effects of anesthesia on heart rate and blood pressure. Therefore, the mean arterial blood pressure was maintained at > 90 mmHg to ensure sufficient brain perfusion. Blood pressure was measured (VP-1000 VET, Votem) with an appropriately sized cuff. After the examination, all dogs were evaluated for their hydration status with physical examination (mild: minimal loss of skin turgor and clinically normal eye; moderate: moderate loss of skin turgor, dry mucous membranes, and enophthalmos; severe: considerable loss of skin turgor, extremely dry mucous membranes, and severely enophthalmos) and provided 0.9% sodium chloride solution IV by maintenance fluid injection rate.
Imaging technique—The dogs were placed in a ventral recumbent position and triangular cushions were used to hold the head to set the brain oblique to the CT beam (Supplementary Figure S1). This position allowed the caudal area from the parietal lobe to be included in the CT (z-axis = 40 mm). All CTs were acquired using a 160-multislice CT scanner (Aquilion Lightening 160; Canon Medical Systems). CT perfusion imaging was performed with 5-mm collimation, 1 pitch, 100 kV tube voltage, tube current 100 mA conditions, and all images were obtained using axial scanning (double-slice technique or double z sampling, 0.5 X 80 row).
Pre-contrast CT was performed before to the brain PCT, and the range was established from the nose to the first cervical vertebrae. Based on the pre-contrast image, a range from the parietal lobe to the cerebellum, including the hippocampus and the occipital lobe, was selected for brain PCT. Then, the contrast medium was injected simultaneously with the start of the PCT, which was performed at 2-second intervals for 50 seconds (Supplementary Figure S2). A nonionic iodinated contrast medium (Omnipaque, GE healthcare, 350 mg I/mL, 350 mg I/kg) was administered through an intravenous catheter using a power injector according to the different conditions mentioned earlier.18 To prevent stagnation of the contrast medium in the cerebral blood vessels, a 5-minute interval was allowed between injections across all injection rates.22 The same procedure was repeated in the second experiment using a 20-gauge catheter. The acquired images were reconstructed with a slice thickness of 1 cm.
Analysis of brain PCT images
Inclusion criteria of TDC—Brain PCT images were evaluated with the use of available software (VITREA® Version 7.14.4, Canon Medical Systems) based on the deconvolution method. The rostral cerebral artery and dorsal sagittal sinus were automatically selected for the regions of interest (ROIs) of TDCs (Figure 1). If the automatic selection of the ROI recognized an incorrect position (eg, bone), re-localization was performed manually.
The shape of the TDC graph was analyzed before performing a quantitative assessment of the TDC parameters to normalize the graph (eg, the bell shape) and to reduce the influence of other variables (eg, cardiac function). Inadequate TDC graphs were excluded according to the following criteria15,23: (1) fluctuating graphs that had incorrect placement of ROI, such as on the bone; (2) graphs that appeared as too slow an upstroke with a broad-based curve due to the low cardiac output; and (3) graphs with multiple peaks due to respiratory motion (Supplementary Figure S3). In excluded cases, the same procedure was repeated a month after the second experiment.
Quantitative analysis of TDC parameters—All TDC parameters were measured in seconds. The parameters measured on the TDC graph included the initiation ta, tv, peak Tap, and Tvp (Figure 1). Based on these values, the differences between Tap and tv (Tap – tv) and between Tap and ta (Tap – ta) were calculated. All parameters were measured in each experiment, and the mean values were used for statistical analysis.
Measurements of perfusion mapping parameters—Based on the TDC results, 5 perfusion mapping parameters, namely, CBV, the ratio of the area under the tissue curve and the area under the curve of the vein), time to peak of tissue (TTP), CBF, the ratio of CBV and MTT), MTT and Tmax were measured (Figure 2). All these parameters were measured under conditions that were verified as reliable combinations of injection rate and catheter size based on the experimental results.
As mentioned above, the cerebellum was evaluated and analyzed by dividing it into 4 parts: the rostral vermis, caudal vermis, and left and right cerebellar hemispheres. Additionally, other regions known to be sensitive to ischemia, such as the parietal lobe, hippocampus, and occipital lobe, were evaluated. These areas were drawn by free hand on one side, and the mirror image function was used to estimate the opposite side of the same level symmetrically. All anatomic regions were determined as in previous studies.24,25
Statistical analysis
All data were presented as the mean ± SD and were measured 3 times by one observer. Quantitative analysis of the perfusion parameters was performed using the Mann–Whitney H and Mann–Whitney U tests. All statistical analyses were performed using SPSS ver. 27 (SPSS Inc.); P < .05 was considered statistically significant.
Results
Physiological evaluation of animals
The mean age of all dogs was 14.4 months, and the mean weight was 8.9 ± 0.7 kg. They were considered clinically normal on the basis of the results of several examinations mentioned earlier.
The heart rate and mean arterial blood pressure (MAP) were decreased after the induction of anesthesia. Temporarily, MAP values ≤ 80 mmHg were observed in 2 dogs during the second experiment. The anesthetic depth was immediately controlled in these 2 dogs, and the experiment was resumed after the MAP was normalized. In the recovery phase, 1 dog was administered atropine (0.04 mL/kg, IV) due to a temporary drop in blood pressure, and the MAP was normalized to > 90 mmHg. All dogs recovered normally after anesthesia.
TDC parameters among 3 different injection rates with the same catheter size
The total injection time of the contrast medium ranged from 5.8 seconds to 7.1 seconds at 2 mL/second, 3.9 seconds to 4.7 seconds at 3 mL/second, and 2.9 s to 3.5 s at 4 mL/second. In the 24-gauge catheter size, both Tap-tv and Tap-ta were significantly (P < .05) shorter in the 3 mL/second than in 2 mL/second (Table 1). There was no significant difference (P = .242 to .829) in the results for the 4 remaining parameters.
Comparison of the mean ± SD results for time-density curve (TDC) variables among 3 different injection rates (2, 3, or 4 mL/second) for the administration of non-ionic contrast medium (Omnipaque, GE Healthcare; 350 mg I/mL; 350 mg I/kg, IV) through a 24-gauge catheter to evaluate the effect of contrast medium injection rates and IV catheter sizes on PCT of brains of clinically normal 5-year-old sexually intact male Beagles in a cross-over study conducted between February 28 and April 26, 2022.
Injection rate (mL/s) | P-value | ||||
---|---|---|---|---|---|
Parameter | 2 | 3 | 4 | 2 mL/s vs 3 mL/s | 3 mL/s vs 4 mL/s |
ta (s) | 10.8 ± 1.7 | 10.4 ± 3.2 | 7.5 ± 1.0 | .439 | .107 |
tv (s) | 13.2 ± 2.2 | 12.8 ± 3.0 | 11.0 ± 2.0 | .829 | .519 |
Tap (s) | 24.8 ± 3.3 | 21.6 ± 4.0 | 19.0 ± 2.5 | .242 | .379 |
Tvp (s) | 28.0 ± 4.0 | 24.8 ± 4.8 | 23.0 ± 4.1 | .242 | .617 |
Tap – tv (s) | 11.6 ± 1.6* | 8.8 ± 1.0* | 8.0 ± 1.6 | .021 | .411 |
Tap – ta (s) | 14.0 ± 2.0* | 11.2 ± 1.0* | 11.5 ± 1.9 | .033 | .893 |
Compared results in the row differed significantly.
ta = Initiation time of arterial inflow. Tap = Peak time of arterial enhancement. tv = Initiation time of venous outflow. Tvp = Peak time of venous enhancement.
There was no significant difference (P = .107 to .893) for results between the injection rate of 3 mL/second and 4 mL/second with the 24-gauge catheter and among the 3 injection rates with the 20-gauge catheter (Table 1; Table 2). At an injection rate of 4 mL/second with a 24-gauge catheter, IV catheter rupture or leakage of contrast medium occurred in 4 of the 5 dogs.
Comparison of the mean ± SD results for TDC variables when a 20-gauge IV catheter was used for administering the contrast medium at 3 different injection rates (2, 3, or 4 mL/second) as described in Table 1.
Injection rate (mL/s) | P-value | ||||
---|---|---|---|---|---|
Parameter | 2 | 3 | 4 | 2 mL/s vs 3 mL/s | 3 mL/s vs 4 mL/s |
ta (s) | 8.0 ± 2.0 | 6.8 ± 2.2 | 6.0 ± 3.7 | .381 | .517 |
tv (s) | 10.0 ± 2.0 | 8.8 ± 2.2 | 8.0 ± 3.7 | .381 | .517 |
Tap (s) | 20.8 ± 3.3 | 18.0 ± 3.7 | 16.4 ± 4.5 | .161 | .606 |
Tvp (s) | 23.6 ± 4.3 | 20.4 ± 4.5 | 19.2 ± 5.4 | .161 | .337 |
Tap – tv (s) | 10.8 ± 1.7 | 9.2 ± 1.7 | 8.8 ± 1.7 | .142 | .522 |
Tap – ta (s) | 12.8 ± 1.7 | 11.8 ± 1.7 | 10.4 ± 0.8 | .142 | .439 |
Data are presented as the mean ± SD.
See Table 1 for key.
TDC parameters in the different catheter sizes under the same injection rates
Results for the same parameters were analyzed according to different catheter sizes (24-gauge and 20-gauge) under the same injection rate. Mean ± SD of ta was significantly (P = .045) shorter when a 20-gauge catheter (8.0 ± 2.0 seconds) vs in 24-gauge catheter (10.8 ± 1.7 seconds) was used for the contrast medium injection rate of 2 mL/second (Table 3). There were no significant (P = .045 to .817) differences in the results for other TDC parameters across injection rates (2, 3, or 4 mL/second).
Comparison of the mean ± SD results for TDC variables when 24-gauge vs 20-gauge IV catheters were used for the administration of contrast medium in the study described in Table 1.
2 mL/s | 3 mL/s | 4 mL/s | |||||||
---|---|---|---|---|---|---|---|---|---|
Parameter | 24-gauge | 20-gauge | P-value | 24-gauge | 20-gauge | P-value | 24-gauge | 20-gauge | P-value |
ta (s) | 10.8 ± 1.7 | 8.0 ± 2.0 | .045 | 10.4 ± 3.2 | 6.8 ± 2.2 | .083 | 7.5 ± 1.0 | 6.0 ± 3.7 | .205 |
tv (s) | 13.2 ± 2.2 | 10.0 ± 2.0 | .055 | 12.8 ± 3.0 | 8.8 ± 2.2 | .055 | 11.0 ± 2.0 | 8.0 ± 3.7 | .205 |
Tap (s) | 24.8 ± 3.3 | 20.8 ± 3.3 | .089 | 21.6 ± 4.0 | 18.0 ± 3.7 | .105 | 19.0 ± 2.5 | 16.4 ± 4.5 | .213 |
Tvp (s) | 28.0 ± 4.0 | 23.6 ± 4.3 | .136 | 24.8 ± 4.8 | 20.4 ± 4.5 | .070 | 23.0 ± 4.1 | 19.2 ± 5.4 | .217 |
Tap – tv (s) | 11.6 ± 1.6 | 10.8 ± 1.7 | .343 | 8.8 ± 1.0 | 9.2 ± 1.7 | .811 | 8.0 ± 1.6 | 8.8 ± 1.7 | .561 |
Tap – ta (s) | 14.0 ± 2.0 | 12.8 ± 1.7 | .282 | 11.2 ± 1.0 | 11.8 ± 1.7 | .817 | 11.5 ± 1.9 | 10.4 ± 0.8 | .306 |
See Table 1 for key.
Brain perfusion mapping parameters
Results for perfusion mapping parameters were evaluated for an injection rate of 3 mL/second with a 24-gauge catheter based on the above experimental results. The mean ± SD results for CBV, TTP, CBF, MTT, and Tmax were compiled for regions of interest (Table 4).
Mean ± SD results of perfusion mapping parameters of the cerebellum and other (ROI) for the dogs described in Table 1 after administration of contrast medium at an injection rate of 3 mL/second with a 24-gauge catheter.
ROI | CBV (mL/100 g) | TTP (s) | CBF (mL/100 g/min) | MTT (s) | Tmax (s) |
---|---|---|---|---|---|
Rostral vermis | 5.9 ± 0.7 | 23.7 ± 3.6 | 118.0 ± 14.6 | 3.1 ± 0.5 | 2.0 ± 0.2 |
Caudal vermis | 5.6 ± 1.4 | 24.1 ± 3.6 | 103.2 ± 16.7 | 3.5 ± 0.6 | 2.3 ± 0.3 |
Right cerebellar hemisphere | 6.4 ± 1.0 | 23.7 ± 4.0 | 122.7 ± 8.9 | 3.1 ± 0.5 | 2.0 ± 0.3 |
Left cerebellar hemisphere | 6.3 ± 1.1 | 23.8 ± 4.1 | 118.4 ± 12.4 | 3.2 ± 0.3 | 2.0 ± 0.2 |
Parietal lobe | 5.2 ± 1.0 | 24.2 ± 3.8 | 98.5 ± 10.0 | 3.5 ± 0.3 | 2.3 ± 0.2 |
Hippocampus | 6.2 ± 1.2 | 24.0 ± 3.8 | 115.0 ± 22.3 | 3.3 ± 0.6 | 2.1 ± 0.3 |
Occipital lobe | 5.2 ± 0.6 | 23.1 ± 3.1 | 101.3 ± 16.3 | 3.3 ± 0.5 | 2.2 ± 0.3 |
CBF = cerebral blood flow. CBV = cerebral blood volume. MTT = mean transit time. ROI = regions of interest. Tmax = time-to-maximum of the residual function. TTP = time to peak of tissue.
Discussion
The variables influencing the results of brain PCT in small dogs are yet to be clarified. This study found that the injection rate of the contrast medium influenced the time of venous outflow and arterial peak enhancement in the TDC graph. With a 24-gauge catheter size, Tap – tv and Tap – ta were significantly shorter at an injection rate of 3 mL/second than at 2 mL/second. This result indicated that a 3 mL/second flow rate using a 24-gauge catheter allowed the contrast medium to stay in the brain tissue for a sufficient amount of time. Given the stability and reproducibility of these protocols, they could be optimal brain PCT protocols in small-breed dogs. This study also presents valuable data by providing the median reference range of perfusion parameters in Beagles for evaluating perfusion status in brain areas where ischemic changes frequently occur.
If the blood-brain barrier is not compromised, the contrast medium flows into the artery (first pass), passes through the brain tissue, and flows into the vein (wash-out).26 Given that PCT indirectly reflects perfusion status through the flow of the contrast medium in the brain, a certain amount of time is required for sufficient retention of the contrast medium in the brain tissue. To satisfy this assumption, TDC should reach the arterial peak time quickly while the initiation time of venous outflow should be slow. Therefore, an injection rate of 3 mL/second was considered closer to the ideal conditions than 2 mL/second with the 24-gauge catheter.
In this study, most TDC parameters tended to be shorter at an injection rate of 4 mL/second than at a rate of 3 mL/second, but no significant differences were found between them. In addition, an injection rate of 4 mL/second using a 24-gauge catheter resulted in leakage of the contrast medium and IV catheter rupture. A high injection pressure exceeding 10,342 hPa applied to the IV catheter is associated with a potential risk of rupture or damage to the catheter and extravasation of the contrast medium, which reduces the accuracy of the perfusion results.16 To overcome this, a large IV catheter to resist rapid injection has been recommended in several studies in humans10; however, the application of large catheters is limited in small animals. Our results indicated that a 4 mL/second injection rate using a 24-gauge catheter was not suitable with respect to the stability and safety of PCT scanning.
Similarly, in the 20-gauge catheter, the overall TDC parameters decreased as the injection rate increased; however, there were no significant differences among the different 3 injection rates. Therefore, in the 20-gauge catheter size, the injection rate did not affect the TDC parameters.
When comparing 24-gauge and 20-gauge catheters under the same injection rates, only ta was significantly shorter in the 20-gauge catheter than in the 24-gauge catheter at a 2 mL/second injection rate. Parameters ta is influenced by various factors, such as cardiac output function, heart rate, and blood pressure.12 Therefore, it was difficult to evaluate which IV catheter size condition was close to the ideal one according to the difference of the single parameter.
Theoretically, based on the maximum slope model, a very rapid injection rate of 20 mL/second is required to shorten the time to reach the arterial peak value in humans.10 However, a highly rapid injection rate also has several disadvantages including increased risks of extravasation or local leakage of the contrast medium and vascular wall rupture.13,27 Therefore, the clinical application of brain PCT is difficult, and studies using relatively low injection rates have been performed. These studies demonstrated that flow rates under 10 mL/second are sufficient without any substantial compromise in perfusion image quality.28,29
Additionally, with the development of the deconvolution analysis method, it is possible to obtain accurate results even with a low injection rate, such as 3–4 mL/second.27 A study using the deconvolution method validated its efficacy in animals with a low injection rate.30 However, to the best of our knowledge, the current study is the first to evaluate, using the deconvolution method, the effects of different injection rates and catheter sizes on TDC and PCT results in Beagles.
Two studies16,17 in veterinary medicine have also analyzed the effects of variables related to contrast medium injection on PCT; however, the results have varied. One study demonstrated that rapid administration of contrast medium is required for the quantitative analysis of hepatic PCT.17 Conversely, another study reported that even a low contrast medium injection rate of 1.5 mL/second is sufficient for the evaluation of renal perfusion.16 The current study found that the contrast medium injection rate affected brain PCT when a 24-gauge was used. These conflicting results could be due to the differences in the detailed conditions of scanning, target organs for imaging, and analysis software used.
With respect to the median reference range of the 5 perfusion parameters with a 24-gauge catheter and an injection rate of 3 mL/second, the average values of CBV and CBF in this study were higher than those in previous studies on dogs and rabbits.31,32 This could be associated with the development of CT imaging techniques and different scanning conditions.
Perfusion mapping parameters are related to brain autoregulation mechanisms.2 In the infarction core, a reduced CBF leads to a reduced CBV. However, in the penumbra, while the CBF is also decreased as in the infarction core, the CBV is in the normal range or is mildly increased as a compensatory mechanism.2
In human medicine, the diagnosis of ischemic stroke using PCT is generally performed by comparing the hemodynamic changes in the perfusion parameters with reference to those in the normal contralateral hemisphere or by comparing the changing ratio based on normal thresholds. Although absolute reference values for normal perfusion in the brain are known, a relative comparison of each value is considered a more reliable and reproducible method in humans.9 Therefore, in the same sense, this median range was recommended for use as relative reference values to compare normal and abnormal ischemic tissues, rather than absolute thresholds.
This study has some limitations. First, the interobserver reproducibility of the perfusion mapping parameters was not evaluated in this study. However, several studies have indicated good interobserver reliability among experienced radiologists in the evaluation of PCT in human medicine.33,34 Second, the effects of anesthesia on TDC graphs and perfusion imaging were not considered. Isoflurane, the study anesthetic, interferes with cerebral vasodilation and decreases cerebral metabolism and functional activity.35–37 It is also known to increase CBF and disrupt cerebral autoregulation.38 Some studies in monkeys have shown that CBF is significantly increased in the cerebrum, medulla, and cerebellum under a high dose (2.0%) of isoflurane.39 Third, the contrast medium was injected using a single injector. Therefore, sufficient saline was not injected to push the contrast medium. In addition, the 5-minute interval between the administrations of the contrast medium may be insufficient for a complete wash-out. Despite these limitations, this study provides the median reference range of perfusion parameters in the brain regions known to be sensitive to ischemic changes. Further studies that consider the study limitations are required to confirm our results and to evaluate the applicability of PCT for evaluating cerebrovascular events are needed.
In conclusion, a PCT scanning protocol of an injection rate of 3 mL/second using a 24-gauge catheter size has reliable stability and reproducibility in small breed dogs. PCT with this technique will be a useful diagnostic tool for evaluating brain perfusion status in small dogs.
Supplementary Materials
Supplementary materials are posted online at the journal website: avmajournals.avma.org.
Acknowledgments
We thank Canon Medical Systems Korea, especially Sean Kang (CT application specialist), for assistance with image acquisition and technical cooperation.
The authors declare that there were no conflicts of interest and there was no external funding in this study.
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