• View in gallery

    Transverse CTA images of the sinus of the pulmonary trunk (A through C), caudal lobe branch of the left pulmonary artery (D through F), and accessory lobe branch of the right pulmonary artery (G through I) at airway pressures of 0 (A, D, G), 10 (B, E, H), and 20 (C, F, I) cm H2O. Notice the contrast enhancement of the pulmonary artery at each airway pressure (arrow). Arterial enhancement was low and heterogeneous at 20 cm H2O, compared with at 0 and 10 cm H2O.

  • View in gallery

    Transverse CTA images of the sinus of the pulmonary trunk (A through C), middle lobe branch of the right pulmonary artery (D through F), and caudal lobe branch of the left pulmonary artery (G through I) at airway pressures of 0 (A, D, G), 10 (B, E, H), and 20 (C, F, I) cm H2O. Notice the change in diameter of the pulmonary artery as airway pressure increases (arrow).

  • 1. Goggs R, Chan DL, Benigni L, et al. Comparison of computed tomography pulmonary angiography and point-of-care tests for pulmonary thromboembolism diagnosis in dogs. J Small Anim Pract 2014;55:190197.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 2. Wittram C, Maher MM, Yoo AJ, et al. CT angiography of pulmonary embolism: diagnostic criteria and causes of misdiagnosis. Radiographics 2004;24:12191238.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 3. Ngwenyama TR, Herring JM, O'Brien M, et al. Contrast-enhanced multidetector computed tomography to diagnose pulmonary thromboembolism in an awake dog with pyothorax. J Vet Emerg Crit Care (San Antonio) 2014;24:731738.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 4. Schoepf UJ, Costello P. CT angiography for diagnosis of pulmonary embolism: state of the art. Radiology 2004;230:329337.

  • 5. Goggs R, Benigni L, Fuentes VL, et al. Pulmonary thromboembolism. J Vet Emerg Crit Care (San Antonio) 2009;19:3052.

  • 6. Drees R, Francois CJ, Saunders JH. Invited review—computed tomographic angiography (CTA) of the thoracic cardiovascular system in companion animals. Vet Radiol Ultrasound 2014;55:229240.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 7. Habing A, Coelho JC, Nelson N, et al. Pulmonary angiography using 16 slice multidetector computed tomography in normal dogs. Vet Radiol Ultrasound 2011;52:173178.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 8. Drees R, Frydrychowicz A, Keuler NS, et al. Pulmonary angiography with 64-multidetector-row computed tomography in normal dogs. Vet Radiol Ultrasound 2011;52:362367.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 9. Makara M, Dennler M, Kühn K, et al. Effect of contrast medium injection duration on peak enhancement and time to peak enhancement of canine pulmonary arteries. Vet Radiol Ultrasound 2011;52:605610.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 10. Behrendt FF, Jost G, Pietsch H, et al. Computed tomography angiography: the effect of different chaser flow rates, volumes, and fluids on contrast enhancement. Invest Radiol 2011;46:271276.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 11. Raczeck P, Minko P, Graeber S, et al. Influence of respiratory position on contrast attenuation in pulmonary CT angiography: a prospective randomized clinical trial. AJR Am J Roentgenol 2016;206:481486.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 12. Wittram C, Yoo AJ. Transient interruption of contrast on CT pulmonary angiography: proof of mechanism. J Thorac Imaging 2007;22:125129.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 13. Renne J, Falck CV, Ringe KI, et al. CT angiography for pulmonary embolism detection: the effect of breathing on pulmonary artery enhancement using a 64-row detector system. Acta Radiol 2014;55:932937.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 14. Kuzo RS, Pooley RA, Crook JE, et al. Measurement of caval blood flow with MRI during respiratory maneuvers: implications for vascular contrast opacification on pulmonary CT angiographic studies. AJR Am J Roentgenol 2007;188:839842.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 15. Mortimer AM, Singh RK, Hughes J, et al. Use of expiratory CT pulmonary angiography to reduce inspiration and breath-hold associated artefact: contrast dynamics and implications for scan protocol. Clin Radiol 2011;66:11591166.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 16. Powell FL, Wagner PD, West JB. Ventilation, blood flow, and gas exchange. In: Broaddus VC, Mason RJ, Ernst JD, et al, eds. Murray and Nadel's textbook of respiratory medicine. 6th ed. Philadelphia: WB Saunders Co, 2016;44–75.

    • Search Google Scholar
    • Export Citation
  • 17. Garcia JGN. Pulmonary circulation and regulation of fluid balance. In: Broaddus VC, Mason RJ, Ernst JD, et al, eds. Murray and Nadel's textbook of respiratory medicine. 6th ed. Philadelphia: WB Saunders Co, 2016;92–110.

    • Search Google Scholar
    • Export Citation
  • 18. Patel S, Kazerooni EA, Cascade PN. Pulmonary embolism: optimization of small pulmonary artery visualization at multi-detector row CT. Radiology 2003;227:455460.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 19. Miller WT Jr, Marinari LA, Barbosa E Jr, et al. Small pulmonary artery defects are not reliable indicators of pulmonary embolism. Ann Am Thorac Soc 2015;12:10221029.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 20. Bae KT. Intravenous contrast medium administration and scan timing at CT: considerations and approaches. Radiology 2010;256:3261.

  • 21. Guarracino A, Lacitignola L, Auriemma E, et al. Which airway pressure should be applied during breath-hold in dogs undergoing thoracic computed tomography? Vet Radiol Ultrasound 2016;57:475481.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 22. Scharf SM, Caldini P, Ingram RH Jr. Cardiovascular effects of increasing airway pressure in the dog. Am J Physiol 1977;232:H35H43.

  • 23. Sakai S, Yabuuchi H, Chishaki A, et al. Effect of cardiac function on aortic peak time and peak enhancement during coronary CT angiography. Eur J Radiol 2010;75:173177.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 24. Bae KT, Heiken JP, Brink JA. Aortic and hepatic contrast medium enhancement at CT. Part II. Effect of reduced cardiac output in a porcine model. Radiology 1998;207:657662.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 25. Scott JC, Finkelstein LJ, Croll MN. Effects of hypoxemia on coronary blood flow and cardiac output in normal and hypothyroid dogs. Am J Cardiol 1962;10:840845.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 26. Pinsky MR. Recent advances in the clinical application of heart-lung interactions. Curr Opin Crit Care 2002;8:2631.

  • 27. Fessler HE, Brower RG, Wise RA, et al. Effects of positive end-expiratory pressure on the canine venous return curve. Am Rev Respir Dis 1992;146:410.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 28. Berger D, Moller PW, Weber A, et al. Effect of PEEP, blood volume, and inspiratory hold maneuvers on venous return. Am J Physiol Heart Circ Physiol 2016;311:H794H806.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 29. Moore NR, Scott JP, Flower CD, et al. The relationship between pulmonary artery pressure and pulmonary artery diameter in pulmonary hypertension. Clin Radiol 1988;39:486489.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 30. Kallas HJ, Domino KB, Glenny RW, et al. Pulmonary blood flow redistribution with low levels of positive end-expiratory pressure. Anesthesiology 1998;88:12911299.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 31. Levitzky MG. Chapter 4. Blood flow to the lung. In: Levitzky MG, ed. Pulmonary physiology. 8th ed. New York: The McGraw-Hill Co, 2013;97–103.

    • Search Google Scholar
    • Export Citation
  • 32. Tidwell SA, Graham JP, Peck JN, et al. Incidence of pulmonary embolism after non-cemented total hip arthroplasty in eleven dogs: computed tomographic pulmonary angiography and pulmonary perfusion scintigraphy. Vet Surg 2007;36:3742.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 33. Wittram C. How I do it: CT pulmonary angiography. AJR Am J Roentgenol 2007;188:12551261.

  • 34. Hunsaker AR, Oliva IB, Cai T, et al. Contrast opacification using a reduced volume of iodinated contrast material and low peak kilovoltage in pulmonary CT angiography: objective and subjective evaluation. AJR Am J Roentgenol 2010;195:W118W124.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 35. Rodrigues JC, Mathias H, Negus IS, et al. Intravenous contrast medium administration at 128 multidetector row CT pulmonary angiography: bolus tracking versus test bolus and the implications for diagnostic quality and effective dose. Clin Radiol 2012;67:10531060.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 36. Hopper K, Powell LL. Basics of mechanical ventilation for dogs and cats. Vet Clin North Am Small Anim Pract 2013;43:955969.

  • 37. MacDonnell KF, Lefemine AA, Moon HS, et al. Comparative hemodynamic consequences of inflation hold, PEEP, and interrupted PEEP: an experimental study in normal dogs. Ann Thorac Surg 1975;19:552560.

    • Crossref
    • Search Google Scholar
    • Export Citation

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Effects of airway pressure on contrast enhancement and diameter of the pulmonary artery in healthy dogs as determined by use of computed tomography angiography

Sangkyung Choen DVM1, Kitae Kim DVM1, Kyuyong Kang DVM1, Jiwon Kang DVM1, Jihye Nam DVM1, Junghee Yoon DVM, PhD1, and Mincheol Choi DVM, PhD1
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  • 1 1Department of Veterinary Medical Imaging, College of Veterinary Medicine and Research Institute for Veterinary Science, Seoul National University, 1 Gwanak-ro, Gwanak-gu, Seoul 08826, Republic of Korea.

Abstract

OBJECTIVE

To evaluate effects of airway pressure on contrast enhancement and diameter of the pulmonary artery and determine the optimal airway pressure for pulmonary CT angiography in dogs.

ANIMALS

8 healthy Beagles.

PROCEDURES

Thoracic CT was performed at end-expiration (0 cm H2O) and 2 positive-pressure end-inspirations (10 and 20 cm H2O). Attenuation curves of enhancement for the sinus of the pulmonary trunk artery were obtained by use of a bolus technique. Contrast medium (300 mg of I/kg) was administered IV, and CT imaging began at the time of peak enhancement. At each pressure, time to peak enhancement, ratio of blood flow from the caudal vena cava to the right side of the heart (KCdVC), and enhancement characteristics and diameter changes of the pulmonary artery were evaluated.

RESULTS

All dogs had a significant delay for time to peak enhancement in the sinus of the pulmonary trunk artery as airway pressure increased. The KCdVC progressively increased as airway pressure increased, and there was low contrast enhancement and increased pulmonary artery filling defects at 20 cm H2O. All pulmonary arteries had marked increases in diameter as pressure increased. Arterial distensibility in the gravity-dependent cranial lung region was greater than that in the gravity-independent caudal lung region at the 2 positive-pressure end-inspirations.

CONCLUSIONS AND CLINICAL RELEVANCE

Airway pressure affected time to peak enhancement, KCdVC, contrast enhancement, and pulmonary artery diameter. Results suggested that 10 cm H2O could be an optimal pressure for evaluation of the pulmonary artery of dogs by use of CT angiography. (Am J Vet Res 2019;80;756–763)

Abstract

OBJECTIVE

To evaluate effects of airway pressure on contrast enhancement and diameter of the pulmonary artery and determine the optimal airway pressure for pulmonary CT angiography in dogs.

ANIMALS

8 healthy Beagles.

PROCEDURES

Thoracic CT was performed at end-expiration (0 cm H2O) and 2 positive-pressure end-inspirations (10 and 20 cm H2O). Attenuation curves of enhancement for the sinus of the pulmonary trunk artery were obtained by use of a bolus technique. Contrast medium (300 mg of I/kg) was administered IV, and CT imaging began at the time of peak enhancement. At each pressure, time to peak enhancement, ratio of blood flow from the caudal vena cava to the right side of the heart (KCdVC), and enhancement characteristics and diameter changes of the pulmonary artery were evaluated.

RESULTS

All dogs had a significant delay for time to peak enhancement in the sinus of the pulmonary trunk artery as airway pressure increased. The KCdVC progressively increased as airway pressure increased, and there was low contrast enhancement and increased pulmonary artery filling defects at 20 cm H2O. All pulmonary arteries had marked increases in diameter as pressure increased. Arterial distensibility in the gravity-dependent cranial lung region was greater than that in the gravity-independent caudal lung region at the 2 positive-pressure end-inspirations.

CONCLUSIONS AND CLINICAL RELEVANCE

Airway pressure affected time to peak enhancement, KCdVC, contrast enhancement, and pulmonary artery diameter. Results suggested that 10 cm H2O could be an optimal pressure for evaluation of the pulmonary artery of dogs by use of CT angiography. (Am J Vet Res 2019;80;756–763)

Pulmonary thromboembolism is a condition characterized by partial or complete obstruction of the pulmonary artery or its branches by a thrombus.1 In humans, diagnostic tests for thromboembolic disease include assay of D-dimer concentrations, ventilation-perfusion scintigraphy, and various pulmonary angiographies, including selective or nonselective angiography, CTA, and magnetic resonance angiography.2,3 Currently, CTA of the pulmonary artery is noninvasive, can be rapidly performed, and is the most commonly used first-choice diagnostic test for patients with suspected pulmonary thromboembolism.3,4 However, in veterinary medicine, there currently is no criterion-referenced diagnostic test for pulmonary thromboembolism. Moreover, thoracic radiography is still indicated for diagnostic imaging of pulmonary thromboemboli in dogs, even though radiographic findings in affected dogs with pulmonary thromboembolism are often nonspecific and vary from no abnormalities to evidence of pulmonary infiltration.5

The increase in availability of multidetectorrow CT scanners has allowed for rapid acquisition of images with high temporal and spatial resolution.6 Furthermore, the introduction of this advanced imaging technique into veterinary medicine has increased interest in the evaluation of pulmonary thromboembolism in dogs by the use of CTA, and several pulmonary studies3,6–10 have been conducted with CTA. In these studies, contrast enhancement of the pulmonary vessels was dependent on several factors, including injection rate and duration of injection, concentration of contrast medium, use of a flushing solution after injection of contrast medium, and delay of the scan time.6–10 Although several CTA protocols have been used to achieve sufficient contrast enhancement in the pulmonary arteries of humans, a false-negative diagnosis of pulmonary thromboembolism has been reported as a result of low contrast enhancement of the pulmonary arteries during image acquisition.11

Results of some studies11–15 have indicated that respiratory status also can influence contrast enhancement in pulmonary CTA. Changes in airway pressure can affect diameter and flow velocity of the CdVC.14 An increase in unopacified blood from the CdVC, which results in dilution of the contrast column, could cause poor contrast enhancement during pulmonary CTA.14,15

Pulmonary vasculature can be physiologically subdivided into alveolar and extra-alveolar vessels. Alveolar vessels are exposed directly to alveolar pressure, whereas extra-alveolar vessels are extremely sensitive to the state of lung inflation.16 Changes in airway pressure can affect the transmural pressure of each pulmonary vessel; transmural pressure is related to the diameters of the alveolar and extra-alveolar vessels.17 When the lungs inflate, increased surface tension in the layers of the alveolar lining causes a decrease in the diameters of alveolar vessels. In contrast, radial traction of the surrounding alveolar walls causes the diameters of extra-alveolar vessels to increase.16 It is thought that increasing the diameters of extra-alveolar vessels, including pulmonary arteries and veins, could lead to better imaging of the lobar arteries and an increase in the number of visible segmental and subsegmental arteries, which could improve the sensitivity for diagnosis of pulmonary thromboembolism.18,19

The purpose of the study reported here was to evaluate the effect of airway pressure on time to peak enhancement, KCdVC, and characteristics of contrast enhancement and diameter of the pulmonary artery. These results then could be used to determine an optimal airway pressure for pulmonary CTA in dogs. We hypothesized that changes in airway pressure would affect contrast enhancement and diameter of the pulmonary arteries.

Materials and Methods

Animals

Eight 3-year-old Beagles (2 females and 6 males) were used in the study. Body weight of the dogs ranged from 6.1 to 14.5 kg. The dogs were considered to be healthy on the basis of results of physical examinations, CBCs, biochemical and electrolyte analyses, thoracic radiography, and echocardiography. There were no clinical signs of cardiovascular or respiratory problems. All dogs had negative results when tested for heartworm infection; dogs received drugs for heartworm prevention every month. Dogs were cared for in accordance with guidelines for the Laboratory Animal Research Center, and the study protocol was approved by the Institutional Animal Care and Use Committee of Seoul National University (SNU-180709-1-1).

Anesthesia

Food but not water was withheld from all dogs for at least 12 hours before induction of anesthesia for CT imaging. Dogs were sedated by administration of acepromazine (0.01 mg/kg, IV). Anesthesia was induced with alfaxalone (2.0 mg/kg, IV), which was administered through a 22-gauge catheter into a cephalic vein. Dogs were endotracheally intubated, and anesthesia was maintained with isoflurane in oxygen. During anesthesia and CTA, electrocardiography, pulse oximetry, capnography, and noninvasively measured systolic, diastolic, and mean arterial blood pressures were continuously monitored (ie, oscillometric technique) with a multiparametric monitor.

CTA

Three distinct ventilation pressures were used for each dog. Dogs were positioned in sternal recumbency on the CT table and manually hyperventilated to induce transient apnea as a result of a decrease in end-tidal partial pressure of CO2. The CT images were obtained at end-expiration (0 cm H2O) and 2 positive-pressure end-inspirations (10 and 20 cm H2O); manual compression of a reservoir bag was used to achieve each end-inspiration pressure. Breath holding was maintained until CT images were obtained. For each dog, ventilation pressures were applied in the order of 0, 10, and 20 cm H2O. Each pressure was administered on a separate day, with a minimum interval of 1 week between successive pressure administrations.

A 22-gauge catheter was placed in the cephalic vein of the right forelimb for each of the 3 pressure administrations. After unenhanced CT images were obtained, time to peak enhancement was determined through analysis of time-attenuation curves by use of a test bolus technique. For each ventilation pressure, a bolus (4 mL) of iodinated contrast mediuma was injected automatically by a power injector at a rate of 2 mL/s within the maximum pressure limit of 1,379 hPa. Repeated transverse plane cine images (120 kV, 50 mA·s, slice thickness of 4 mm, and tube rotation time of 0.75 seconds), which were obtained beginning simultaneously with injection of the contrast medium, were acquired over the mediastinum and transecting the base of the sinus of the pulmonary trunk. Images were obtained at intervals of 1 second for 25 seconds. Time to peak enhancement in the sinus of the pulmonary trunk was analyzed on the scanner by drawing a circular or oval region of interest.

After the test bolus evaluation was completed, pulmonary CTA was performed. For each airway pressure, each dog received contrast medium (300 mg of I/kg) by use of the same injection rate used for the test bolus technique. Images of the thorax were obtained at the time of peak enhancement in the sinus of the pulmonary trunk. Images were acquired with a 64-row multidetector CT scannerb in a craniocaudal direction from the thoracic inlet to the caudal aspect of the diaphragm by use of the following settings: slice thickness, 1 mm; pitch, 0.828; rotation duration, 0.5 seconds; tube voltage, 120 kV; and tube current, 200 mA. For each dog, time for acquisition of CT images was consistent for the 3 pressure administrations. During CT imaging, heart rate, mean arterial blood pressure, and hemoglobin oxygen saturation were recorded for each dog.

Image analysis

All transverse, sagittal, and dorsal enhanced CT images were reconstructed for analysis. Images were viewed in the pulmonary embolic-specific window (width, 700 HU; level, 100 HU) and lung window (width, 1,500 HU; level, −600 HU) by use of image analysis software.c

Quantitative measurements of attenuation were obtained in the right ventricle, CrVC, CdVC, and sinus of the pulmonary trunk. For each analysis, a circular or oval region of interest in each anatomic area was standardized to between 100 and 200 mm2 for the right ventricle, 50 and 100 mm2 for the sinus of the pulmonary trunk, and 20 and 30 mm2 for the CrVC and CdVC.

For evaluation of the KCdVC, which could have influenced contrast enhancement of pulmonary arteries, attenuation values were obtained in the CrVC, CdVC, and right ventricle as previously described. To minimize partial volume effects, measurements were obtained on 3 consecutive transverse images in each anatomic location, and a mean value was calculated to provide a weighted average of the attenuation in each location.

The KCdVC was calculated by equating attenuation in the right ventricle to a weighted average attenuation of the CrVC and CdVC, assuming that the CrVC and CdVC were the sole contributors of flow to the right side of the heart,12 by use of the following equation:

article image

where CRV is attenuation of the right ventricle, CCdVC is the weighted average attenuation of the CdVC, and CCrVC is the weighted average attenuation of the CrVC.

The value for KCdVC then was determined by use of the following equation:

article image

Three veterinary radiologists evaluated contrast enhancement and diameters of 10 pulmonary arteries, including the sinus of the pulmonary trunk, right pulmonary artery and its branches (the cranial lobe, middle lobe, caudal lobe, and accessory lobe branches), and left pulmonary artery and its branches (the caudal lobe branch and the ascending and descending branches of the cranial lobe branch). The radiologists were not aware of the airway pressure administered to each dog. Each radiologist obtained each measurement 3 times without consulting the other radiologists, and the mean of these 9 measurements was calculated and used for analysis. All measurements were obtained at the same anatomic location in the transverse images.

In addition to evaluating contrast enhancement in the sinus of the pulmonary trunk, heterogeneous contrast-filling defects in each pulmonary artery were evaluated on dorsal, sagittal, and transverse images. A quality score of contrast enhancement was assigned on the basis of the number of contrast-filling defects in the pulmonary arteries by use of a 5-point scale as follows: 5 = 0 to 2 defects, 4 = 2 to 4 defects, 3 = 4 to 6 defects, 2 = 6 to 8 defects, and 1 = 8 to 10 defects.

The diameter of each of the 10 pulmonary arteries was measured with built-in electronic calipers at a location immediately proximal to the first bifurcation of each pulmonary artery. The smallest diameter of the pulmonary arteries identified in cross section on CT images was measured to eliminate effects of oblique views on the determination of actual arterial diameters. When the pulmonary arteries were viewed in long-axis orientation on CT images, diameter was measured at the largest width. For each airway pressure, the number of pulmonary arteries < 3 mm in diameter was counted in all 80 pulmonary arteries of the 8 dogs.

Additionally, lung lobes were anatomically subdivided into 3 regions that comprised the cranial (cranial lobe of the right lung and cranial part of the cranial lobe of the left lung), middle (middle lobe of the right lung and caudal part of the cranial lobe of the left lung), and caudal (caudal lobe of the right lung, accessory lobe, and caudal lobe of the left lung) lung regions. Arterial distensibility between end-expiration (0 cm H2O) and end-inspiration (10 and 20 cm H2O) for each lung region was compared by use of the following equation:

Arterial distensibility = ([pulmonary arterial diameter during end-inspiration - pulmonary arterial diameter during end-expiration]/pulmonary arterial diameter during end-expiration) × 100.

Statistical analysis

Data were analyzed with commercially available software.d The Friedman test was used to determine differences in physiologic variables (heart rate, mean arterial blood pressure, and hemoglobin oxygen saturation), time to peak enhancement after bolus injection, and KCdVC for the 3 airway pressures. The same statistical analysis was used to determine differences in the degree and quality score of contrast enhancement and the diameter of the pulmonary arteries for the 3 airway pressures.

The Friedman test was also used to determine differences among mean pulmonary arterial distensibility of the 3 anatomic lung regions. When significant differences were detected, the Wilcoxon signed rank test with Bonferroni-Holm multiple-comparisons adjustment was performed to determine significant differences between each of the 3 possible pairs of airway pressures.

Intraclass correlation coefficients were calculated to evaluate interobserver agreement. Intraclass correlation coefficient values < 0.59 were considered poor, values between 0.60 and 0.79 were considered fair, and values between 0.80 and 1.00 were considered excellent.

Results were reported as mean ± SD. Values of P < 0.05 were considered significant.

Results

No clinical problems were associated with anesthesia or CT imaging. Image acquisition time ranged from 5.3 to 6.3 seconds (mean ± SD, 5.68 ± 0.35 seconds). Heart rate, mean arterial blood pressure, and hemoglobin oxygen saturation during CT imaging did not differ significantly among the 3 airway pressures (Table 1). As airway pressure increased, the time to peak enhancement after bolus injection was significantly (P = 0.01) delayed (mean ± SD delay of 4.00 ± 1.41 seconds for 0 cm H2O, 5.50 ± 1.60 seconds for 10 cm H2O, and 8.75 ± 1.67 seconds for 20 cm H2O).

Table 1—

Mean ± SD values for cardiovascular variables of 8 dogs during breath holding at 3 airway pressures during pulmonary CTA.

Airway pressure (cm H2O)Heart rate (beats/min)Mean arterial blood pressure (mm Hg)Hemoglobin oxygen saturation (%)
0119 ± 1656 ± 998 ± 1
10118 ± 1155 ± 1098 ± 1
20119 ± 2164 ± 2097 ± 1

The CTA images of contrast enhancement of the pulmonary arteries for each airway pressure were obtained (Figure 1). The KCdVC was calculated for each airway pressure. Dogs had a significant (P = 0.01) increase in KCdVC as airway pressure increased. The mean ± SD KCdVC for airway pressures of 0, 10, and 20 cm H2O was 0.62 ± 0.09, 0.76 ± 0.11, and 0.85 ± 0.06, respectively. Contrast enhancement and quality score were significantly lower at 20 cm H2O, compared with results for the other airway pressures (Table 2). However, contrast enhancement and quality score were not significantly different between airway pressures of 0 and 10 cm H2O.

Figure 1—
Figure 1—

Transverse CTA images of the sinus of the pulmonary trunk (A through C), caudal lobe branch of the left pulmonary artery (D through F), and accessory lobe branch of the right pulmonary artery (G through I) at airway pressures of 0 (A, D, G), 10 (B, E, H), and 20 (C, F, I) cm H2O. Notice the contrast enhancement of the pulmonary artery at each airway pressure (arrow). Arterial enhancement was low and heterogeneous at 20 cm H2O, compared with at 0 and 10 cm H2O.

Citation: American Journal of Veterinary Research 80, 8; 10.2460/ajvr.80.8.756

Table 2—

Mean ± SD values for contrast enhancement of the sinus of the pulmonary trunk and quality score of 10 pulmonary arteries of 8 dogs at 3 airway pressures.

 Airway pressure (cm H2O)
Variable01020
Contrast enhancement (HU)541.57 ± 78.06a593.66 ± 111.87a369.25 ± 60.77b
Quality score5.00 ± 0a4.88 ± 0.35a3.13 ± 0.64b

Quality score was assigned on the basis of the number of contrast-filling defects in the pulmonary arteries by use of a 5-point scale as follows: 5 = 0 to 2 defects, 4 = 2 to 4 defects, 3 = 4 to 6 defects, 2 = 6 to 8 defects, and 1 = 8 to 10 defects.

Within a row, values with different superscript letters differ significantly (P < 0.05; Wilcoxon signed rank test with Bonferroni-Holm multiple-comparisons adjustment).

Diameter of each of the 10 pulmonary arteries was measured at all 3 airway pressures (Table 3). Diameters of each of the 10 pulmonary arteries differed significantly (P < 0.001) among the 3 airway pressures. In all dogs, diameter of each of the pulmonary arteries increased as airway pressure increased (Figure 2). For all 8 dogs, the total number of pulmonary arteries < 3 mm in diameter was 16, 8, and 1 at 0, 10, and 20 cm H2O, respectively.

Figure 2—
Figure 2—

Transverse CTA images of the sinus of the pulmonary trunk (A through C), middle lobe branch of the right pulmonary artery (D through F), and caudal lobe branch of the left pulmonary artery (G through I) at airway pressures of 0 (A, D, G), 10 (B, E, H), and 20 (C, F, I) cm H2O. Notice the change in diameter of the pulmonary artery as airway pressure increases (arrow).

Citation: American Journal of Veterinary Research 80, 8; 10.2460/ajvr.80.8.756

Table 3—

Mean ± SD diameter (mm) of the pulmonary arteries of 8 dogs at 3 airway pressures.

 Airway pressure (cm H2O)
Artery01020
Sinus of the pulmonary trunk11.51 ± 1.18a12.87 ± 0.83b14.83 ± 1.40c
Right pulmonary artery5.84 ± 0.66a6.70 ± 0.71b7.45 ± 0.88c
Cranial lobe branch3.07 ± 0.35a3.55 ± 0.47b4.05 ± 0.56c
Middle lobe branch3.33 ± 0.39a3.75 ± 0.40b4.16 ± 0.48c
Caudal lobe branch5.52 ± 0.77a5.89 ± 0.81b6.40 ± 0.92c
Accessory lobe branch3.40 ± 0.38a3.65 ± 0.35b3.99 ± 0.34c
Left pulmonary artery5.79 ± 0.49a6.88 ± 0.58b7.79 ± 0.84c
Ascending branch of the cranial lobe branch3.26 ± 0.97a3.66 ± 1.06b4.11 ± 1.25c
Descending branch of the cranial lobe branch2.82 ± 0.18a3.12 ± 0.27b3.46 ± 0.39c
Caudal lobe branch5.53 ± 0.61a5.99 ± 0.66b6.56 ± 0.74c

Within a row, values with different superscript letters differ significantly (P < 0.05; Wilcoxon signed rank test with Bonferroni-Holm multiple-comparisons adjustment).

Distensibility of the pulmonary arteries in each anatomic lung region was determined for airway pressures of 10 and 20 cm H2O (Table 4). Arterial distensibility of lobes in the cranial lung region was significantly greater than that in the caudal lung region.

Table 4—

Mean ± SD distensibility of the pulmonary arteries between end-expiration (0 cm H2O) and positive-pressure end-inspiration (10 and 20 cm H2O) airway pressures for 3 anatomic lung regions of 8 dogs.

 
Airway pressure (cm H2O)CranialMiddleCaudal
1014 ± 3a12 ± 6ab7 ± 4b
2029 ± 6a24 ± 7ab18 ± 4b

Values reported are percentages and were calculated as ([pulmonary arterial diameter during end-inspiration – pulmonary arterial diameter during end-expiration]/pulmonary arterial diameter during end-expiration) × 100.

Lung lobes were anatomically subdivided into 3 regions as follows: cranial = cranial lobe of the right lung and cranial part of the cranial lobe of the left lung, middle = middle lobe of the right lung and caudal part of the cranial lobe of the left lung, and caudal = caudal lobe of the right lung, accessory lobe, and caudal lobe of the left lung.

Within a row, values with different superscript letters differ significantly (P < 0.05; Wilcoxon signed rank test with Bonferroni-Holm multiple-comparisons adjustment).

Interobserver reliability scores were derived for contrast enhancement of the sinus of the pulmonary trunk, quality score, and diameters of the pulmonary arteries (Table 5). Interobserver reliability was excellent for all 3 variables assessed.

Table 5—

Intraclass correlation coefficients of interobserver reliability scores (3 observers) for the evaluation of contrast enhancement, quality score, and diameter of pulmonary arteries.

 Airway pressure (cm H2O)
Variable01020
Contrast enhancement0.9450.9880.953
Quality score0.8750.8810.963
Diameter0.9850.9870.987

Coefficient values < 0.59 were considered poor, values between 0.60 and 0.79 were considered fair, and values between 0.80 and 1.00 were considered excellent.

Discussion

Results of the study reported here indicated that changes in airway pressure had 3 main effects on pulmonary arteries, as assessed by use of CTA. First, time to peak enhancement of the sinus of the pulmonary trunk was significantly delayed as airway pressure increased. Second, KCdVC increased as airway pressure increased, with a significantly lower degree and quality of contrast enhancement at 20 cm H2O. Third, all pulmonary arteries had a marked increase in diameter as airway pressure increased. Specifically, arteries in the cranial lung region had more prominent distension than did those in the caudal lung region.

Time to peak enhancement is determined by factors associated with the contrast medium (eg, injection volume and rate of injection) and patient (eg, cardiac output and venous access).9,20 In the present study, factors associated with contrast medium and venous access for placement of a catheter in a cephalic vein were consistent for each dog for each of the 3 airway pressures. Although there was no significant difference in physiologic factors (ie, heart rate, mean arterial blood pressure, and hemoglobin oxygen saturation) among the 3 airway pressures, a relationship between positive airway pressures and cardiac outputs has been detected. Increases in pleural pressure and pulmonary vascular resistance that occur during lung expansion by use of positive-pressure ventilation cause an increase in right atrial pressure, which results in a reduction in central venous return, stroke volume, and cardiac output.21,22 Additionally, a strong negative correlation between cardiac output and time to peak enhancement has been detected in previous studies23,24 that involved the use of CT. Consequently, time to peak enhancement in the present study would have been delayed in response to the increase in airway pressure.

In the study reported here, KCdVC was calculated on the basis of the assumption that the right side of the heart receives blood only from the CrVC and CdVC.12 This is an acceptable assumption because coronary circulation constitutes only 3.31% of cardiac output in anesthetized dogs.12,25 In the present study, KCdVC increased significantly as intrathoracic airway pressure increased. There are possible mechanisms that could explain venous return to the right side of the heart. When the lungs expand during positive-pressure airway ventilation, caudal displacement of the diaphragm would simultaneously cause an increase in abdominal pressure, which would contribute to a greater impetus for venous return through the CdVC.12 In addition, although positive-pressure end-expiration ventilation decreases blood flow to the liver in proportion to decreases in cardiac output in normovolemic dogs, the hepatic blood flow is unchanged.26 Increases in abdominal pressure by caudal displacement of the diaphragm may be the major mechanism by which a decrease in venous return through the CdVC is minimized during positive-pressure ventilation.26,27 Investigators of another study28 also reported that patterns of decrease and recovery of blood flow differed between the CrVC and CdVC during positive-pressure ventilation. Although blood flow in the CdVC initially decreased more than that in the CrVC, it recovered more completely and extremely rapidly (within a few heartbeats) in that study.28 In the present study, breath holding for > 9 seconds could have caused complete recovery of blood flow from the CdVC during CT scanning.

The degree and quality score of contrast enhancement were significantly lower at 20 cm H2O than at 0 and 10 cm H2O; however, there was not a significant difference in the degree and quality score of contrast enhancement between 0 and 10 cm H2O. Interdependence between cardiac output and KCdVC could have resulted in differences in contrast enhancement among the 3 airway pressures. Although a decrease in cardiac output reportedly causes an increase in peak arterial enhancement,24 the increase in KCdVC in the study reported here could have offset the effect of a decrease in cardiac output at the airway pressure of 10 cm H2O. Alternatively, the effect of the increase in the KCdVC could have exceeded that of a decrease in cardiac output at the airway pressure of 20 cm H2O, which resulted in low contrast enhancement. It has been suggested that dilution of contrast agents as a result of an increase in unopacified blood from the CdVC could cause transient interruption of contrast enhancement and low contrast enhancement during pulmonary CTA.11,12,14 In humans, the inferior vena cava contributes approximately 80% of the total flow in patients in whom low contrast enhancement in the pulmonary artery is detected.13 The mean KCdVC of the present study was > 0.8 only at the airway pressure of 20 cm H2O with lower contrast enhancement.

Diameter of the pulmonary arteries is influenced by changes in transmural pressure and blood flow.29 On a physiologic basis, vessels of the pulmonary circulation are categorized into 2 types, extra-alveolar and alveolar vessels. During inflation of the lungs, alveolar vessels are compressed and elongated, which causes transmural pressure in the alveolar vessels to decrease. In contrast, the interstitial pressure surrounding extra-alveolar vessels decreases with inflation of the lungs, which causes dilation of extra-alveolar vessels.17 Results of 1 study19 indicated that the presence of pulmonary thromboemboli progressively decreased with decreasing diameter of pulmonary vascular lesions and that pulmonary arterial diameters < 3 mm had higher false-positive and false-negative rates, compared with rates for those > 3 mm in diameter. In the present study, diameter of the pulmonary arteries increased as airway pressure increased. For the 8 dogs, the total number of pulmonary arteries < 3 mm in diameter was 16, 8, and 1 at pressures of 0, 10, and 20 cm H2O, respectively. These findings could be used to reduce the likelihood of false-positive and false-negative diagnoses of pulmonary thrombi in small peripheral vessels, which may be inadequate for evaluating pulmonary embolisms at an airway pressure of 0 cm H2O.19

Evaluation of the degree of arterial distensibility of the 3 anatomic lung regions revealed some remarkable findings. In the study reported here, lobes located in the cranial lung region had a greater degree of arterial distensibility than did lobes located in the caudal lung region. Generally, the cranial lung region in dogs in sternal recumbency is considered to be a more gravity-dependent region than is the caudal lung region. In the present study, an increase in airway pressure could have caused an increase in the ventral (dependent)-to-dorsal gradient of pulmonary blood flow, which may have led to a redistribution of blood flow from the non-dependent portion of the lungs to the dependent portion of the lungs.30 This change in pulmonary blood flow could have been a result of the passive distribution of blood flow along the hydrostatic gradient attributable to gravity.30 Also, regional distribution of blood flow can be influenced by cardiac output and pulmonary vascular resistance.30,31

In other studies1,3,7,8,32 involving pulmonary CTA of dogs, the dose of contrast medium was higher than the dose (300 mg of I/kg) used in the study reported here. Doses for those studies ranged from 400 to 1,400 mg of I/kg. Although the minimal enhancement level required for diagnostic CTA is controversial, the theoretical minimum enhancement level required to enable clinicians to see all acute and chronic pulmonary thromboemboli was 211 HU in 1 study.33 In the present study, we used a lower contrast dose than that used in previous studies; however, contrast enhancement for all of the airway pressures was > 250 HU, which is thought to be sufficient for detection of pulmonary thromboemboli.34 In the present study, this result may have been achieved by an optimal delay for CT imaging and more rapid image acquisition (mean ± SD, 5.68 ± 0.35 seconds). Moreover, the test bolus technique used in the present study could have provided higher attenuation of the pulmonary arteries, compared with results for a bolus tracking technique.35

In general, a low airway pressure between 8 and 15 cm H2O is required for anesthetized patients with clinically normal lungs, and pressures between 10 and 12 cm H2O have been recommended to improve lung aeration during breath holding.21,36 At an airway pressure of 0 cm H2O, a focal increase in vascular resistance caused by an increase in lung atelectasis could result in misdiagnosis of pulmonary emboli owing to unenhanced or poorly enhanced blood within the affected vessel mimicking a pulmonary embolism.2,21 In the present study, no pressure-related complications were identified during CT imaging. However, it is possible that a pressure of 20 cm H2O could cause an increase in pulmonary arterial pressure of up to 15 mm Hg and result in lung hyperinflation.21,37

The present study had several limitations. First, only 3 airway pressures were used, which limited the identification of the most appropriate airway pressure for pulmonary CTA. Second, we did not perform direct measurements of cardiac output and blood inflow to the right side of the heart from the CrVC, CdVC, and coronary vein. In addition, the contribution of coronary blood flow to the right side of the heart was considered minimal and excluded from the calculation of KCdVC. However, changes in coronary blood flow caused by differences in airway pressure could also have affected KCdVC. Third, in contrast to results for healthy dogs, positive-pressure ventilation could cause a different cardiopulmonary response and impose adverse cardiovascular effects in affected dogs. Finally, the small sample size and use of a single breed should also be considered when interpreting these results.

In the study reported here, changes in airway pressure affected the time to peak enhancement, contrast enhancement characteristics, and diameter of the pulmonary arteries in dogs evaluated by use of CTA. Therefore, in clinical practice, the cardiovascular effects of different airway pressures should be considered when performing pulmonary CTA. It was also found that the number of contrast-filling defects of the pulmonary arteries was significantly increased at an airway pressure of 20 cm H2O. Moreover, diameter of the pulmonary arteries was smaller at 0 cm H2O. On the basis of these findings, an airway pressure of 10 cm H2O could be optimal for performing pulmonary CTA of dogs.

Acknowledgments

Supported in part by the Research Institute for Veterinary Science at Seoul National University. Funding sources did not have any involvement in the study design, data analysis and interpretation, or writing and publication of the manuscript.

The authors declare that there were no conflicts of interest.

ABBREVIATIONS

CdVC

Caudal vena cava

CrVC

Cranial vena cava

CTA

CT angiography

KCdVC

Ratio of blood flow from the caudal vena cava to the right side of the heart

Footnotes

a.

Omnipaque 300, GE Healthcare, Cork, Ireland.

b.

Aquillion 64, Toshiba Medical Systems Corp, Ötawara, Japan.

c.

INFINITT, Infinitt Healthcare Co Ltd, Seoul, Republic of Korea.

d.

IBM SPSS Statistics for Windows, version 23.0, IBM Corp, Armonk, NY.

References

  • 1. Goggs R, Chan DL, Benigni L, et al. Comparison of computed tomography pulmonary angiography and point-of-care tests for pulmonary thromboembolism diagnosis in dogs. J Small Anim Pract 2014;55:190197.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 2. Wittram C, Maher MM, Yoo AJ, et al. CT angiography of pulmonary embolism: diagnostic criteria and causes of misdiagnosis. Radiographics 2004;24:12191238.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 3. Ngwenyama TR, Herring JM, O'Brien M, et al. Contrast-enhanced multidetector computed tomography to diagnose pulmonary thromboembolism in an awake dog with pyothorax. J Vet Emerg Crit Care (San Antonio) 2014;24:731738.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 4. Schoepf UJ, Costello P. CT angiography for diagnosis of pulmonary embolism: state of the art. Radiology 2004;230:329337.

  • 5. Goggs R, Benigni L, Fuentes VL, et al. Pulmonary thromboembolism. J Vet Emerg Crit Care (San Antonio) 2009;19:3052.

  • 6. Drees R, Francois CJ, Saunders JH. Invited review—computed tomographic angiography (CTA) of the thoracic cardiovascular system in companion animals. Vet Radiol Ultrasound 2014;55:229240.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 7. Habing A, Coelho JC, Nelson N, et al. Pulmonary angiography using 16 slice multidetector computed tomography in normal dogs. Vet Radiol Ultrasound 2011;52:173178.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 8. Drees R, Frydrychowicz A, Keuler NS, et al. Pulmonary angiography with 64-multidetector-row computed tomography in normal dogs. Vet Radiol Ultrasound 2011;52:362367.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 9. Makara M, Dennler M, Kühn K, et al. Effect of contrast medium injection duration on peak enhancement and time to peak enhancement of canine pulmonary arteries. Vet Radiol Ultrasound 2011;52:605610.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 10. Behrendt FF, Jost G, Pietsch H, et al. Computed tomography angiography: the effect of different chaser flow rates, volumes, and fluids on contrast enhancement. Invest Radiol 2011;46:271276.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 11. Raczeck P, Minko P, Graeber S, et al. Influence of respiratory position on contrast attenuation in pulmonary CT angiography: a prospective randomized clinical trial. AJR Am J Roentgenol 2016;206:481486.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 12. Wittram C, Yoo AJ. Transient interruption of contrast on CT pulmonary angiography: proof of mechanism. J Thorac Imaging 2007;22:125129.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 13. Renne J, Falck CV, Ringe KI, et al. CT angiography for pulmonary embolism detection: the effect of breathing on pulmonary artery enhancement using a 64-row detector system. Acta Radiol 2014;55:932937.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 14. Kuzo RS, Pooley RA, Crook JE, et al. Measurement of caval blood flow with MRI during respiratory maneuvers: implications for vascular contrast opacification on pulmonary CT angiographic studies. AJR Am J Roentgenol 2007;188:839842.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 15. Mortimer AM, Singh RK, Hughes J, et al. Use of expiratory CT pulmonary angiography to reduce inspiration and breath-hold associated artefact: contrast dynamics and implications for scan protocol. Clin Radiol 2011;66:11591166.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 16. Powell FL, Wagner PD, West JB. Ventilation, blood flow, and gas exchange. In: Broaddus VC, Mason RJ, Ernst JD, et al, eds. Murray and Nadel's textbook of respiratory medicine. 6th ed. Philadelphia: WB Saunders Co, 2016;44–75.

    • Search Google Scholar
    • Export Citation
  • 17. Garcia JGN. Pulmonary circulation and regulation of fluid balance. In: Broaddus VC, Mason RJ, Ernst JD, et al, eds. Murray and Nadel's textbook of respiratory medicine. 6th ed. Philadelphia: WB Saunders Co, 2016;92–110.

    • Search Google Scholar
    • Export Citation
  • 18. Patel S, Kazerooni EA, Cascade PN. Pulmonary embolism: optimization of small pulmonary artery visualization at multi-detector row CT. Radiology 2003;227:455460.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 19. Miller WT Jr, Marinari LA, Barbosa E Jr, et al. Small pulmonary artery defects are not reliable indicators of pulmonary embolism. Ann Am Thorac Soc 2015;12:10221029.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 20. Bae KT. Intravenous contrast medium administration and scan timing at CT: considerations and approaches. Radiology 2010;256:3261.

  • 21. Guarracino A, Lacitignola L, Auriemma E, et al. Which airway pressure should be applied during breath-hold in dogs undergoing thoracic computed tomography? Vet Radiol Ultrasound 2016;57:475481.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 22. Scharf SM, Caldini P, Ingram RH Jr. Cardiovascular effects of increasing airway pressure in the dog. Am J Physiol 1977;232:H35H43.

  • 23. Sakai S, Yabuuchi H, Chishaki A, et al. Effect of cardiac function on aortic peak time and peak enhancement during coronary CT angiography. Eur J Radiol 2010;75:173177.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 24. Bae KT, Heiken JP, Brink JA. Aortic and hepatic contrast medium enhancement at CT. Part II. Effect of reduced cardiac output in a porcine model. Radiology 1998;207:657662.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 25. Scott JC, Finkelstein LJ, Croll MN. Effects of hypoxemia on coronary blood flow and cardiac output in normal and hypothyroid dogs. Am J Cardiol 1962;10:840845.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 26. Pinsky MR. Recent advances in the clinical application of heart-lung interactions. Curr Opin Crit Care 2002;8:2631.

  • 27. Fessler HE, Brower RG, Wise RA, et al. Effects of positive end-expiratory pressure on the canine venous return curve. Am Rev Respir Dis 1992;146:410.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 28. Berger D, Moller PW, Weber A, et al. Effect of PEEP, blood volume, and inspiratory hold maneuvers on venous return. Am J Physiol Heart Circ Physiol 2016;311:H794H806.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 29. Moore NR, Scott JP, Flower CD, et al. The relationship between pulmonary artery pressure and pulmonary artery diameter in pulmonary hypertension. Clin Radiol 1988;39:486489.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 30. Kallas HJ, Domino KB, Glenny RW, et al. Pulmonary blood flow redistribution with low levels of positive end-expiratory pressure. Anesthesiology 1998;88:12911299.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 31. Levitzky MG. Chapter 4. Blood flow to the lung. In: Levitzky MG, ed. Pulmonary physiology. 8th ed. New York: The McGraw-Hill Co, 2013;97–103.

    • Search Google Scholar
    • Export Citation
  • 32. Tidwell SA, Graham JP, Peck JN, et al. Incidence of pulmonary embolism after non-cemented total hip arthroplasty in eleven dogs: computed tomographic pulmonary angiography and pulmonary perfusion scintigraphy. Vet Surg 2007;36:3742.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 33. Wittram C. How I do it: CT pulmonary angiography. AJR Am J Roentgenol 2007;188:12551261.

  • 34. Hunsaker AR, Oliva IB, Cai T, et al. Contrast opacification using a reduced volume of iodinated contrast material and low peak kilovoltage in pulmonary CT angiography: objective and subjective evaluation. AJR Am J Roentgenol 2010;195:W118W124.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 35. Rodrigues JC, Mathias H, Negus IS, et al. Intravenous contrast medium administration at 128 multidetector row CT pulmonary angiography: bolus tracking versus test bolus and the implications for diagnostic quality and effective dose. Clin Radiol 2012;67:10531060.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 36. Hopper K, Powell LL. Basics of mechanical ventilation for dogs and cats. Vet Clin North Am Small Anim Pract 2013;43:955969.

  • 37. MacDonnell KF, Lefemine AA, Moon HS, et al. Comparative hemodynamic consequences of inflation hold, PEEP, and interrupted PEEP: an experimental study in normal dogs. Ann Thorac Surg 1975;19:552560.

    • Crossref
    • Search Google Scholar
    • Export Citation

Contributor Notes

Address correspondence to Dr. Choi (mcchoi@snu.ac.kr).