• View in gallery

    Transverse thoracic CT images of 6 foals of a variety of ages (2 [A], 5 [B], 6 [C], 8 [D], 11 [E], and 13 [F] days) at the same anatomic location showing an increase in attenuation of the lung parenchyma and a patchy alveolar pattern in the ventral portion of the lung.

  • View in gallery

    Distribution of mean CT attenuation values of the whole lung for foals ≤ 7 days of age (squares; n = 5) and foals > 7 but ≤ 14 days of age (diamonds; 5). Frequency represents the number of voxels of a particular attenuation value. Thus, a higher frequency suggests a higher volume of lung of a particular attenuation value.

  • View in gallery

    Box-and-whisker plots of mean CT attenuation values (HU) along the cranial-to-caudal gradient in the lungs of foals ≤ 7 days of age (solid boxes; n = 5) and foals > 7 but ≤ 14 days of age (dashed boxes; 5). The top and bottom of each box represent the 25th to 75th percentiles, the central line represents the 50th percentile, the bottom whiskers represent 0th to 25th percentiles, and the top whiskers represent the 75th to 100th percentiles. aIndicated value is significantly (P < 0.05) different from corresponding point 4 value. bIndicated value is significantly (P < 0.05) different from the corresponding values at points 4, 5, and 6. cIndicated value is significantly (P < 0.05) different from the corresponding point 8 value. dIndicated value is significantly (P < 0.05) different from the corresponding point 7 value.

  • View in gallery

    Box-and-whisker plots of mean CT attenuation values (HU) along the ventral-to-dorsal gradient in the lungs of the foals in Figure 3. a–eWithin a foal group, values with different letters are significantly (P < 0.05) different.

  • View in gallery

    Distribution of relative gas (gray bars) and tissue (black bars) volumes along the cranial-to-caudal (A) and ventral-to-dorsal (B) gradients in all foals represented in Figures 3 and 4. A—ncreased attenuation in the mid lung region corresponds to reductions in measured gas volume relative to tissue volume. B—ncreased attenuation in the ventral lung region corresponds to reductions in measured gas volume relative to tissue volume.

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Qualitative and quantitative interpretation of computed tomography of the lungs in healthy neonatal foals

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  • 1 Department of Veterinary Clinical Medicine, College of Veterinary Medicine, University of Illinois, Urbana, IL 61802.
  • | 2 Department of Veterinary Clinical Medicine, College of Veterinary Medicine, University of Illinois, Urbana, IL 61802.
  • | 3 Department of Veterinary Clinical Medicine, College of Veterinary Medicine, University of Illinois, Urbana, IL 61802.
  • | 4 Department of Veterinary Clinical Medicine, College of Veterinary Medicine, University of Illinois, Urbana, IL 61802.
  • | 5 Department of Veterinary Clinical Medicine, College of Veterinary Medicine, University of Illinois, Urbana, IL 61802.
  • | 6 Department of Veterinary Clinical Medicine, College of Veterinary Medicine, University of Illinois, Urbana, IL 61802.

Abstract

Objective—To qualitatively describe lung CT images obtained from sedated healthy equine neonates (≤ 14 days of age), use quantitative analysis of CT images to characterize attenuation and distribution of gas and tissue volumes within the lungs, and identify differences between lung characteristics of foals ≤ 7 days of age and foals > 7 days of age.

Animals—10 Standardbred foals between 2.5 and 13 days of age.

Procedures—Foals were sedated with butorphanol, midazolam, and propofol and positioned in sternal recumbency for thoracic CT. Image analysis software was used to exclude lung from nonlung structures. Lung attenuation was measured in Hounsfield units (HU) for analysis of whole lung and regional changes in attenuation and lung gas and tissue components. Degree of lung attenuation was classified as follows: hyperinflated or emphysema, −1,000 to −901 HU; well aerated, −900 to −501 HU; poorly aerated, −500 to −101 HU; and nonaerated, > −100 HU.

Results—Qualitative evidence of an increase in lung attenuation and patchy alveolar patterns in the ventral lung region were more pronounced in foals ≤ 7 days of age than in older foals. Quantitative analysis revealed that mean ± SD lung attenuation was greater in foals ≤ 7 days of age (−442 ± 28 HU) than in foals > 7 days of age (−521 ± 24 HU). Lung aeration and gas volumes were lower than in other regions ventrally and in the mid lung region caudal to the heart.

Conclusions and Clinical Relevance—Identified radiographic patterns and changes in attenuation were most consistent with atelectasis and appeared more severe in foals ≤ 7 days of age than in older neonatal foals. Recognition of these changes may have implications for accurate CT interpretation in sedated neonatal foals with pulmonary disease.

Abstract

Objective—To qualitatively describe lung CT images obtained from sedated healthy equine neonates (≤ 14 days of age), use quantitative analysis of CT images to characterize attenuation and distribution of gas and tissue volumes within the lungs, and identify differences between lung characteristics of foals ≤ 7 days of age and foals > 7 days of age.

Animals—10 Standardbred foals between 2.5 and 13 days of age.

Procedures—Foals were sedated with butorphanol, midazolam, and propofol and positioned in sternal recumbency for thoracic CT. Image analysis software was used to exclude lung from nonlung structures. Lung attenuation was measured in Hounsfield units (HU) for analysis of whole lung and regional changes in attenuation and lung gas and tissue components. Degree of lung attenuation was classified as follows: hyperinflated or emphysema, −1,000 to −901 HU; well aerated, −900 to −501 HU; poorly aerated, −500 to −101 HU; and nonaerated, > −100 HU.

Results—Qualitative evidence of an increase in lung attenuation and patchy alveolar patterns in the ventral lung region were more pronounced in foals ≤ 7 days of age than in older foals. Quantitative analysis revealed that mean ± SD lung attenuation was greater in foals ≤ 7 days of age (−442 ± 28 HU) than in foals > 7 days of age (−521 ± 24 HU). Lung aeration and gas volumes were lower than in other regions ventrally and in the mid lung region caudal to the heart.

Conclusions and Clinical Relevance—Identified radiographic patterns and changes in attenuation were most consistent with atelectasis and appeared more severe in foals ≤ 7 days of age than in older neonatal foals. Recognition of these changes may have implications for accurate CT interpretation in sedated neonatal foals with pulmonary disease.

Lung imaging is important in the evaluation of patients with respiratory disease. In human patients, CT has become the preferred imaging modality for various pulmonary diseases.1–5 In veterinary medicine, radiography remains the standard method for imaging the lungs,6,7 although the use of CT for the diagnosis of thoracic disease in dogs and cats has been well described.6–8 In sick equine neonates, respiratory disease is a clinically important factor contributing to illness and death, with immaturity of pulmonary and systemic immunity and concurrent systemic disease such as sepsis predisposing foals to pulmonary disease.9–13

The diagnosis and characterization of respiratory disease in hospitalized foals largely rely on radiographic analysis.9 In sick foals, radiographic disease is most often identified in the caudodorsal and caudoventral aspects of the lungs and is commonly represented by diffuse interstitial13 or combined alveolar-interstitial14 disease. Residual fetal fluid in the distal portion of the airways or interstitium and dependent atelectasis may complicate the accurate interpretation of images because radiographic findings can appear similar in newborn or recumbent neonatal foals.13,14 Radiographic evaluation of healthy foals has revealed clearance of fetal fluid by 6 to 12 hours after birth.13,15,16 Foals may be predisposed to atelectasis as a result of immaturity in lung and chest wall compliance17,18 and possibly in surfactant.19 Radiographically, dependent atelectasis is most commonly identified in the caudoventral lung region.13 Published descriptions of thoracic CT findings in foals are not available for neonates and are limited to a case report20 involving a 4-month-old foal.

Limitations to the use of CT in veterinary species have largely involved financial cost, time required for the procedure, and need for anesthesia. These limitations are particularly pertinent to compromised animals, such as neonatal foals with respiratory disease, in which the potential hazard associated with anesthesia may be perceived to be greater than in healthy subjects. In addition, anesthesia-associated atelectasis,21 which is readily detected with CT, can interfere with accurate evaluation of CT images and characterization of disease distribution and severity.19,22–26

Multidetector CT imaging allows for obtainment of high-resolution whole lung images within seconds2,27 and provides more accurate anatomic and morphological characterization of the components of the lungs, including the airways, vessels, and parenchyma, than other imaging modalities.2 In addition, readily available image-analysis software has expanded the use of CT for 3-D quantitative analysis of the distribution of lung gas and tissue volumes2,3,5 as well for evaluation of lung mechanics and perfusion.5 This has led to improvements in locating pathological changes and characterizing specific parenchymal diseases. Use of CT may also facilitate monitoring of disease progression and response to disease intervention.5

Considerable reductions in the time required for image acquisition has made CT imaging a desirable diagnostic tool for veterinary species, particularly when anesthesia can be avoided. A specially designed restraint device has greatly facilitated CT imaging in awake or minimally sedated cats and small dogs.6,27,28 For safety and practical reasons, larger animals, particularly neonatal foals, cannot undergo imaging when awake; however, the use of short-term IV sedation may provide a safe alternative to anesthesia in this population of animals.

Computed tomographic images of the lungs in sedated, spontaneously breathing neonatal foals have not been described in the veterinary literature. Age-specific characterization of morphological characteristics of the lungs in CT scans of sedated neonatal foals is needed because maturational, positional, or sedation-related artifacts may impact interpretation of CT images. The objectives of the study reported here were to qualitatively describe lung CT images obtained from healthy sedated equine neonates, quantitatively characterize lung aeration and distribution of gas and tissue volumes within the lungs, and identify age-related differences if present. We expected that the sedation protocol used would provide an adequate degree of sedation for CT image acquisition; CT would be well tolerated in sedated foals; atelectasis, if present, would be identified in dependent lung regions and would spatially correspond to increased quantitative measurements of lung attenuation; and younger foals (≤ 7 days of age) would have greater soft tissue attenuation in dependent lung regions and greater degrees of lung attenuation than would older foals (> 7 days of age).

Materials and Methods

Animals—Ten university-owned healthy Standardbred neonatal foals (age range, 2.5 to 13 days; 6 males and 4 females; mean ± SD body weight, 64.7 ± 13.6 kg) were used in the study. Foals were determined to be healthy on the basis of unremarkable findings of physical examination, CBC,a and arterial blood gas analysisb as well as standing bilateral thoracic radiography and ultrasonography performed prior to CT. Samples for blood gas analysis were collected aseptically from a dorsal metatarsal artery with foals in lateral recumbency. Any foal with evidence of disease was excluded from the study. Foals and mares were housed at the University of Illinois Horse Farm and transported to the Veterinary Teaching Hospital the morning of the study. The study protocol was approved by the University of Illinois Institutional Animal Care and Use Committee.

Sedation—A 16-gauge guidewire jugular catheterc was aseptically placed in foals for IV administration of all medications. Immediately prior to CT, foals were given butorphanol tartrated (0.05 mg/kg) and midazolame (0.1 mg/kg). When sedation was evident, foals were positioned on the CT table. When further sedation was required, an additional dose of butorphanol (0.05 mg/kg) and midazolam (0.1 mg/kg) or propofolf (4 mg/kg administered to effect) was administered. Foals breathed spontaneously (ie, without mechanical ventilation) throughout the entire CT procedure. Immediately after CT, foals were transported back to the stall for supervised recovery from sedation.

CT image acquisition—All CT imaging was performed with each foal positioned in sternal recumbency, with the head facing the CT scanner gantry. To ensure standard positioning of all foals, correct orientation of the vertebral borders of the scapulae was confirmed. Images were acquired with a 16-slice helical CT scannerg by use of a detail algorithm and the following settings: 140 kVp, 300 mA, 0.5-second rotation, 0.9 pitch, 0.9-second table speed, 512 × 512 matrix, 30-cm display field of view, 50-cm scan field of view, and 5-mm contiguous slice thickness reconstructed to 0.625 mm for the sagittal and dorsal reformations. Total CT scan duration and total duration on the CT table from positioning to scan completion were recorded for all foals. This technique had been previously validated with 1 healthy foal and 3 hospitalized foals. Images were stored as Digital Imaging and Communications in Medicine (DICOM) files for later analysis.

Subjective analysis of CT images—All CT images were seperately reviewed by a diplomate of the American College of Veterinary Radiology (RTO) and a diplomate of the American College of Veterinary Internal Medicine (KML). A consensus opinion was developed regarding the presence or absence of soft tissue attenuation or any other changes. Review of images was performed without the evaluators aware of the foals’ ages. Regions of attenuation were described by location (ie, dorsal, middle, or ventral lung region; cranial or caudal to heart) and severity (mild, moderate, or marked attenuation).

Quantitative analysis of lung densities and volumes—Quantitative image analysis was performed with the aid of semiautomated software.h Initial 3-D segmentation of the lungs through use of HU thresholds enabled exclusion of lung from nonlung structures. Initial threshold values were extrapolated from those reported for other species,2,3 in which values < −950 HU represent external air and those > −200 HU represent fat, muscle, and bone. Preliminary analysis of foal CT images allowed refinement of these threshold values to −860 HU and −120 HU for semiautomated segmentation. Lung segmentation through the use of semiautomated thresholds may result in exclusion of some lung tissue and inclusion of large vessels or other air-filled structures (eg, trachea, large airways, gas-filled stomach, or small intestine); therefore, additional slice-by-slice manual segmentation was performed to exclude these structures and to include areas of lung measuring > −120 HU, including presumed atelectatic regions. The attenuation values obtained from segmented lung were averaged to obtain mean attenuation values. Attenuation corresponds with lung aeration2,3; therefore, attenuation measurements were used to evaluate the degree of regional and whole lung aeration. Classification of the degree of aeration was based on a standard attenuation scale, with hyperinflated (emphysema) regions between −1,000 and −901 HU, well-aerated regions between −900 and −501 HU, poorly aerated regions between −500 and −101 HU, and nonaerated regions > −100 HU.2,3 Volumes of the respective compartments of aeration (hyperinflated, well aerated, poorly aerated, and nonaerated) were derived from known voxel volume and voxel number within each category of aeration, with voxel volume derived via a software algorithm from standardized values for matrix, field of view, and slice thickness. For example, the volume of a well-aerated region of lung would be calculated as follows:

article image

Volumes of the whole lung or any selected region of lung were also derived in this manner.

Changes in attenuation across the lung were measured along cranial-to-caudal and ventral-to-dorsal gradients. To determine the gradients, for each foal, the CT images were divided to the nearest number of slices into 8 regions moving cranial to caudal and 6 regions moving ventral to dorsal. Gradients were designed by use of the percentage of the total lung rather than specific anatomic landmarks; however, certain regions typically corresponded to regions described in the subjective analysis of the lung images. For example, within the cranial-to-caudal gradient, regions 4 to 5 included the region of lung caudal to the base of the heart. Approximate gas and tissue volumes for each region were also calculated across these gradients as follows:

article image

This formula is based on a standard attenuation scale classifying gas (air) at −1,000 HU and water at 0 HU, with lung tissue assumed to have a radiopacity close to that of water (20 to 40 HU).2,3

For example, a region of lung with an attenuation value of −500 HU would consist of approximately 50% gas and 50% tissue.2,3 An increase in gas volume for a particular region corresponds to a lower attenuation value and a greater degree of lung aeration.

Statistical analysis—The sample size used for the study was determined on the basis of an α value of 0.05, power of 0.8, expected difference between age groups of 50 HU, and SD for each group of 27 HU. The Shapiro-Wilk test was used to evaluate the distribution of data. Results are reported as mean ± SD. Statistical softwarei was used to analyze the data.

Pearson correlation analysis was used to determine whether body weight was correlated with mean lung attenuation or lung volume. Pearson correlation analysis was also used to determine whether Pao2 and lung attenuation or lung volume were correlated. The independent-samples t test was used to identify differences in body weight, total duration of the CT evaluation, total lung attenuation (HU), total lung volume, or percentage of well-aerated lung between foals > 7 days of age and foals ≤ 7 days of age and to determine whether propofol use had an effect on lung radiopacity. The Levene test for homogeneity was used to evaluate data variance.

A repeated-measures general linear model was used to determine whether differences in attenuation existed across the lung with both axial and vertical gradients, within foals and between age groups. The Mauchly test for sphericity was used to evaluate data variance for this analysis. When sphericity was not identified, the Greenhouse-Geisser correction factor was applied. Values of P ≤ 0.05 were used to indicate significance.

Results

Animals—Foals were separated into 2 age groups: ≤ 7 days of age (age range, 2.5 to 6 days; n = 5) and > 7 days of age (age range, 8 to 13 days; 5). Mean ± SD body weight of the younger foals was 63 ± 13.1 kg, and that of the older foals was 66.2 ± 15.4 kg. Body weight was not significantly (P = 0.730) different between age groups. Mean temperature-uncorrected Pao2 and Paco2 for all foals prior to sedation were 77.0 ± 8.3 mm Hg and 40.3 ± 2.9 mm Hg, respectively, and were within published29 and institutional reference limits. There were no significant differences in Pao2 (P = 0.351) or Paco2 (P = 0.694) between age groups.

CT scan procedure—No complications were identified in any of the foals during CT, and recovery from sedation was uniformly unremarkable. The degree of sedation with butorphanol and midazolam alone appeared to differ among foals, with 6 foals (3/age group) requiring administration of propofol for additional sedation to facilitate positioning and prevent movement during CT. The maximum propofol dose administered was 80 mg (range, 40 to 80 mg). Apnea was not observed in any foal. No foal required repeated CT scanning because of motion, and motion artifacts secondary to respiration were minimal on subjectively evaluated images.

The mean total duration of CT, including positioning, scout imaging, and CT scanning, was 6.2 ± 2.2 minutes. Mean duration of the CT scan alone was 35.3 ± 4.3 seconds. No differences were evident in total CT duration (P = 0.700) or CT scan duration (P = 0.097) between age groups or between foals that did and did not receive propofol (P = 0.897).

CT image evaluation—Subjective interpretation of the CT images revealed a gradual and diffuse increase in lung attenuation from dorsal to ventral within the lung parenchyma in all foals, with several foals also having a patchy alveolar pattern in the areas of greatest attenuation. This finding was considered to be most consistent with atelectasis, although the contribution of fluid or underlying pulmonary disease could not be entirely ruled out because, in our experience, these may appear radiographically similar. These changes were most obvious caudal to the heart and more pronounced in foals ≤ 7 days of age than in older foals (Figure 1).

Figure 1—
Figure 1—

Transverse thoracic CT images of 6 foals of a variety of ages (2 [A], 5 [B], 6 [C], 8 [D], 11 [E], and 13 [F] days) at the same anatomic location showing an increase in attenuation of the lung parenchyma and a patchy alveolar pattern in the ventral portion of the lung.

Citation: American Journal of Veterinary Research 74, 9; 10.2460/ajvr.74.9.1239

Mean ± SD lung attenuation for all foals was −478.7 ± 44.8 HU, with most of the lung characterized by CT attenuations within the portion of lung classified as poorly aerated (−500 to −100 HU). No difference was identified in lung attenuation between foals given propofol and those not given propofol (P = 0.600). Mean lung attenuation was significantly (P = 0.001) greater in foals ≤ 7 days of age (−442 ± 28 HU) than in foals > 7 days of age (−521 ± 24 HU; Figure 2). When both age groups were considered together, there was a significant (P = 0.005) correlation between lung attenuation and age of foal (r = 0.81).

Figure 2—
Figure 2—

Distribution of mean CT attenuation values of the whole lung for foals ≤ 7 days of age (squares; n = 5) and foals > 7 but ≤ 14 days of age (diamonds; 5). Frequency represents the number of voxels of a particular attenuation value. Thus, a higher frequency suggests a higher volume of lung of a particular attenuation value.

Citation: American Journal of Veterinary Research 74, 9; 10.2460/ajvr.74.9.1239

Quantitative measurement of the distribution of lung attenuation values along the cranial-to-caudal gradient revealed a significant (P = 0.005) increase in lung attenuation in the mid lung region relative to the cranial and caudal regions, and there was a significant (P = 0.015) difference in the cranial-to-caudal gradient between age groups (Figure 3). Along the ventral-to-dorsal gradient, a significant (P < 0.001) increase in lung attenuation was identified in the ventral portion of the lung (Figure 4). This difference was also significant (P = 0.005) between age groups. When ventral-to-dorsal and cranial-to-caudal gradients were evaluated simultaneously, increased lung attenuation was less pronounced in the cranioventral lung region than in the caudoventral lung region (P = 0.051). Increases in lung attenuation in the mid lung region along the cranial-to-caudal gradient and in the ventral lung region along the ventral-to-dorsal gradient corresponded to decreases in the proportion of the measured gas volume relative to the proportion of the measured tissue volume (Figure 5).

Figure 3—
Figure 3—

Box-and-whisker plots of mean CT attenuation values (HU) along the cranial-to-caudal gradient in the lungs of foals ≤ 7 days of age (solid boxes; n = 5) and foals > 7 but ≤ 14 days of age (dashed boxes; 5). The top and bottom of each box represent the 25th to 75th percentiles, the central line represents the 50th percentile, the bottom whiskers represent 0th to 25th percentiles, and the top whiskers represent the 75th to 100th percentiles. aIndicated value is significantly (P < 0.05) different from corresponding point 4 value. bIndicated value is significantly (P < 0.05) different from the corresponding values at points 4, 5, and 6. cIndicated value is significantly (P < 0.05) different from the corresponding point 8 value. dIndicated value is significantly (P < 0.05) different from the corresponding point 7 value.

Citation: American Journal of Veterinary Research 74, 9; 10.2460/ajvr.74.9.1239

Figure 4—
Figure 4—

Box-and-whisker plots of mean CT attenuation values (HU) along the ventral-to-dorsal gradient in the lungs of the foals in Figure 3. a–eWithin a foal group, values with different letters are significantly (P < 0.05) different.

Citation: American Journal of Veterinary Research 74, 9; 10.2460/ajvr.74.9.1239

Figure 5—
Figure 5—

Distribution of relative gas (gray bars) and tissue (black bars) volumes along the cranial-to-caudal (A) and ventral-to-dorsal (B) gradients in all foals represented in Figures 3 and 4. A—ncreased attenuation in the mid lung region corresponds to reductions in measured gas volume relative to tissue volume. B—ncreased attenuation in the ventral lung region corresponds to reductions in measured gas volume relative to tissue volume.

Citation: American Journal of Veterinary Research 74, 9; 10.2460/ajvr.74.9.1239

Mean ± SD estimated lung volume for all foals was 2.8 ± 0.5 L. Mean lung volume for foals > 7 days of age was 3.1 ± 0.4 L and for foals ≤ 7 days of age was 2.6 ± 0.6 L. No difference was identified in lung volume between age groups (P = 0.452); however, there was a significant (P = 0.033) correlation between lung volume and body weight (r = 0.75). The percentage of total lung volume characterized as well aerated was significantly (P = 0.001) greater in foals > 7 days of age than in foals ≤ 7 days of age (Table 1).

Table 1—

Percentage of total lung tissue characterized as hyperaerated (−1,000 to −901 HU), well aerated (−900 to −501 HU), poorly aerated (−500 to−101 HU), and nonaerated (> −100 HU) in CT lung images of foals ≤ 7 days of age (n = 5) and foals > 7 but ≤ 14 days of age (5).

Degree of aerationAge ≤ 7 dAge > 7 dAll foals
Hyperaerated0.000.010.00
Well aerated43.8166.97*57.18
Poorly aerated55.9633.0242.26
Nonaerated0.230.150.01

Value differs significantly (P = 0.001) from the corresponding value for foals < 7 days of age.

Discussion

Computed tomography of the lungs was well tolerated in all 10 healthy neonatal (≤ 14 days of age) foals with the sedation protocol used in the present study. Subjective evaluation of the CT images revealed increased soft tissue attenuation and patchy alveolar patterns within the ventral aspect of the lung parenchyma, with the greatest increases in attenuation caudal to the heart. These changes were more pronounced in foals ≤ 7 days of age than in older foals and could potentially interfere with accurate characterization of disease severity. In all foals, the subjectively assessed distribution of increases in soft tissue attenuation corresponded to increases in the quantitative measurement of attenuation throughout the lung. Significant age-related differences were detected with quantitative evaluation of lung attenuation values, distribution of lung gas and tissue volumes, and volumes of well-aerated lung.

The greater soft tissue attenuation observed in the ventral lung region versus other regions was presumed to be caused by atelectasis of the dependent lung; however, the contribution of residual fetal pulmonary fluid to that attenuation could not be entirely ruled out, particularly in the youngest of foals. Clearance of fetal pulmonary fluid from the alveoli and interstitium is driven by active sodium absorption via airway epithelial sodium channels30,31 and is expected to be complete within 2 to 6 hours after birth in several species.32,33 The exact kinetics of fluid clearance in foals has not been described, but radiographic detection of fetal pulmonary fluid is possible until 6 to 12 hours after parturition.13,15,16 It is possible that CT is able to allow detection of fetal pulmonary fluid beyond the first 6 to 12 hours after parturition because of the greater diagnostic sensitivity of CT imaging than with other imaging modalities.1–5 To the authors’ knowledge, no studies have been conducted with CT to characterize pulmonary fluid clearance in healthy neonatal foals.

Atelectasis is readily detected by CT22–26,34,35 and is typically found in the dependent portion of the lungs.36–40 Atelectasis can interfere with accurate evaluation of CT images and characterization of disease distribution and severity. A primary reason for the development of atelectasis in patients undergoing CT imaging21 is the use of sedation or anesthesia in spontaneously breathing or ventilated subjects. The onset of atelectasis is rapid, and severity increases with increasing duration of anesthesia or sedation. Compared with adults, anesthetized pediatric and juvenile humans develop atelectasis more rapidly in dependent lung regions.21 In other animals, the ventral lung region represents the thinnest portion of the lung and this region is suggested to be more prone to collapse because it has greater compliance and surface-to-volume ratio than other lung regions.39,41 Mechanisms likely contributing to the increased attenuation and presumed atelectasis in the ventral lung region in the study foals included compression of the dependent (ventral) lung regions by the overlying lung or adjacent heart and the potential impact of the medications used for sedation on ventilation.

The doses of sedatives used in the present study may need to be decreased for use in sick foals undergoing CT imaging; however, the sedation protocol chosen represented drugs and dosages routinely used in hospitalized neonatal foals.42 Propofol, butorphanol, and, to a lesser extent, midazolam have dose- and rate-dependent respiratory depressant properties; propofol in particular can induce apnea.43,44 These depressant properties can decrease a patient's usual ventilatory response to Paco2.43,44 Six of the 10 foals used in the study required propofol prior to starting the CT scan. Interestingly, propofol administration was not associated with worsening of atelectasis or increases in lung attenuation as might be expected if its use exacerbated the respiratory depressant effect of the other medications. This may be because of the small doses of propofol used (0.5 to 1 mg/kg) and a slow rate of administration.

Propofol and midazolam also have skeletal muscle relaxant properties,43,44 and it is plausible that these properties may have led to an increase in chest wall compliance. In neonates of many species, chest wall compliance is typically greater than in more mature individuals18,45 and can be associated with reductions in functional residual capacity.18,45 A further increase in chest wall compliance due to sedation could exacerbate the reduction in functional residual capacity and thus promote atelectasis.18,21

Quantitative measurement of mean lung attenuation for all foals resulted in values (−478.7 ± 44.8 HU) within the lower range of attenuations classified as poorly aerated (−500 to −101 HU). The relative proportion of total lung volume classified as poorly aerated (47%) closely approximated the proportion of well-aerated lung (53%). These attenuation values were greater than those typically reported for humans and other species (–700 and −900 HU), as was the proportion of well-aerated versus poorly aerated lung.22,35,37 Direct comparison of foals from this study with findings in other species must be done with caution because the earlier studies typically involved anesthetized and mechanically ventilated adult subjects imaged at peak inspiration or after lung recruitment maneuvers.2–4,23,25,34,35

Significant changes in quantitatively assessed attenuation values were evident along cranial-to-caudal and ventral-to-dorsal gradients and reflected changes in measured gas volumes as well as the distribution of lung areas with subjectively assessed increased attenuation or presumed atelectasis. As observed in mechanically ventilated adult dogs and cats,22,35 a gradual increase in mean lung attenuation and a corresponding decrease in lung gas volume were evident in all foals along the cranial-to-caudal gradient. The maximum changes in gas volume and attenuation in the foals’ lungs were in the mid lung. This pattern was more pronounced in foals ≤ 7 days of age than in foals > 7 days of age and corresponded to the region of the lungs caudal to the heart base in which the increased soft tissue attenuation of the parenchyma and presumed atelectasis were most prominent. This finding is similar to that observed in dogs that undergo CT scanning in sternal recumbency and may represent compression of the lungs by the heart.39,40

The older group of study foals had lower quantitative lung attenuation values than did the younger group. A similar difference has also been noted in pediatric humans over a much larger age range.46 Respiratory physiologic properties in neonates of several species differ from those of adults because of maturational changes in airway development, lung and chest wall compliance, and breathing strategy,18,31,33,45,46 and CT has been used for evaluation of these differences.46,47 How this phenomenon applies to foals in this study is unknown because the scope of our study was limited to comparisons among neonatal foals (≤ 14 days of age) and did not include evaluation of age-related differences over the first 14 days after birth with each foal used as its own control.

Foals ≤ 7 days of age had greater mean lung attenuation, smaller gas volume, and a greater amount of poorly aerated lung relative to well-aerated lung with quantitative image analysis, compared with foals > 7 days of age. The reasons for these differences are unknown. Although younger neonatal foals may be more prone to the development of atelectasis than older neonatal foals, the potential contribution of residual fetal lung fluid in the youngest foals could not be ruled out. Increases in attenuation in foals ≤ 7 days of age due to atelectasis alone should have corresponded to decreases in lung volume, compared with in foals > 7 days of age, once the influence of body size on lung volume was corrected for. Mean lung volume was smaller in the younger foals; however, this difference was not significant (P = 0.452). The study lacked the power to detect significant volume differences, given that post hoc power analysis revealed that approximately 20 foals/group would have been required for that purpose. Had fetal lung fluid contributed to the increase in attenuation in the ventral lung region, this would have contrasted with radiographic findings in foals that indicate fluid clearance from the ventral lung region precedes clearance from the dorsal lung region15 as well as with findings in other species that fluid clearance is not gravity dependent.48 In addition, because only one of the study foals was < 4 days of age, our findings suggested a longer period for fluid clearance than previously described.13,15,16

The ability of the study foals to breathe fully and maintain appropriate end-expiratory lung volume when sedated and in sternal recumbency was impaired to a greater degree in the younger versus older foal group because of potential differences in chest wall compression and lung compliance between these age groups. The increase in chest wall compression in neonatal foals versus in more mature horses is not as extreme as that reported for other species45; however, a decrease in compliance develops over the first 2 weeks after birth.18 Furthermore, some evidence exists to suggest that specific lung compliance is greater in foals > 7 days of age than in younger foals.18

Use of anesthesia and mechanical ventilation in the present study would have allowed for control of the phase of respiration during image acquisition and potentially minimized the amount of atelectasis that developed.24,25 However, anesthesia is known to result in atelectasis artifacts on CT.22–25,36–38 Furthermore, the advantages of performing CT in neonatal foals involve the speed and ease with which the procedure is performed (< 10 minutes in radiology) and the lower financial cost and avoidance of potential risks associated with anesthesia. Newer CT machines also minimize the influence of phase of respiration through image reconstruction.27

Computed tomographic imaging of the lungs in sedated neonatal foals may serve as a useful diagnostic tool, and the use of quantitative image analysis may enable more objective characterization of pulmonary disease in foals than is currently performed. As predicted, thoracic CT changes most consistent with atelectasis were observed in the dependent portion of the lung and these changes were more pronounced in foals ≤ 7 days of age than in older neonates. Additional studies in newborn foals are needed to better describe the contribution that fetal lung fluid clearance may have on CT images. When interpreting CT images in neonatal foals, clinicians should consider the possibility that sedation and age can contribute to image artifacts such as atelectasis. The degree to which these changes would be more pronounced in a compromised and recumbent neonatal foal is unknown.

ABBREVIATION

HU

Hounsfield unit

a.

Cell-dyn 3700 hematology analyzer, GMI Inc, Ramsey, Minn.

b.

Critical Care Express, Nova Biomedical Inc, Waltham, Mass.

c.

MILA International Inc, Erlanger, Ky.

d.

Butorphic (10 mg/mL), Lloyd Laboratories Inc, Shenandoah, Iowa.

e.

Midazolam, (5 mg/mL), Hospira Inc, Lake Forest, Ill.

f.

PropoFlo (10 mg/mL), Abbott Laboratories, North Chicago, Ill.

g.

GE Healthcare, Chalfont St Giles, Buckinghamshire, England.

h.

Amira, Visage Imaging Inc, San Diego, Calif.

i.

SPSS Inc, version 19.0, SPSS Inc, Chicago, Ill.

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Contributor Notes

Presented in abstract form at the 29th Annual Veterinary Comparative Respiratory Society Symposium, Vienna, November 2011.

Supported by the Morris Animal Foundation.

Address correspondence to Dr. Lascola (klascola@illinois.edu).