The number of reptiles kept as pets has increased considerably during the past several years.1 It is estimated that 2.9 million reptiles are privately owned by people in the United States.2 Among other factors, this increase in popularity is attributable to a change in modern lifestyles and the need for companion animals that require less attention and space than most mammalian pets. Unfortunately, many reptiles are purchased by inexperienced owners who have little knowledge on specific husbandry and environmental requirements of their reptilian pets. Consequently, a higher number of reptiles are being brought to veterinarians, and many of these have diseases that are the result of inappropriate housing and feeding conditions.
Infectious diseases of the lungs play an important role in snakes, especially boids (eg, Boa constrictor or Python spp).3 Common causes for the development of pneumonia are inappropriate temperatures, poor hygiene, parasite infestations, and nutritional deficiencies, all of which can cause disturbances of the immune system.4–6 An unsuitable, small environment that restricts movement is another factor, especially for large snakes.3
In snakes, the lungs are a single-chambered tubular structure with a cranial functional portion and a caudal saclike structure without respiratory function. The functional part consists of a central lumen surrounded by an alveolar parenchyma, which is located deep within the cranial portion and becomes shallower in the caudal portion.7 With the exception of boids, most snakes have only 1 functional lung, with the left lung being a vestigial structure.8,9
A main clinical sign in snakes with respiratory tract disease is severe dyspnea, which is often combined with large amounts of mucus within the trachea and oral cavity. In these affected snakes, a definitive diagnosis is important for the choice of treatments as well as for an appropriate prognosis. An important diagnostic tool is the use of a transtracheal wash to provide specimens for microbial culture,6 but the use of imaging techniques is also recommended.5,10 Although endoscopy has been adequately described in reptiles, noninvasive transglottal imaging of the lungs is not possible in larger snakes because of the diameter of long flexible endoscopes.11 Radiographic examination has been performed,10,12,13 but information on the use of modern noninvasive imaging techniques (such as CT) in reptiles is rare, and such techniques have only been evaluated in tortoises.6,14,15
Computed tomography has many advantages, compared with conventional projection radiography, and is used routinely for the diagnosis of lung disease in mammalian species. The objective of the study reported here was to describe the structure of the lungs in healthy snakes and compare those results with findings in snakes with clinical signs of pneumonia. A second objective was to establish reference values for CT assessments of the lungs in snakes.
Materials and Methods
Animals—Eight healthy Indian pythons (Python molurus) and 5 pythons with evidence of respiratory tract disease were used in the study. All snakes were subjected to a thorough clinical examination, which included determination of general condition, body weight, and body length (length from the snout to cloaca). Feces were examined for parasites (flotation method by use of saturated saline [35% NaCl] solution). Swab specimens were obtained from the choana and cloaca, and a transtracheal wash was performed (injection of sterile 0.9% NaCl solution [5 mL/kg] with subsequent aspiration of this fluid).5 A portion of these samples was staineda and used for cytologic examination. Another portion of the samples was submitted for microbiologic evaluation. Aerobic bacterial culture (incubated at 26°C for 24 hours) was conducted by use of Columbia agar supplemented with defibrinated sheep bloodb and brilliant green agarc; isolates were subsequently differentiated.d Fungal culture (incubated at 26°C for 72 to 120 hours) was conducted by use of Sabouraud dextrose agar.e
The snakes were placed in a stretched position for conventional radiographyf by use of laterolateral and dorsoventral projections.16 To examine the entire extent of the lungs, several radiographs were obtained for each projection. Radiographs for snakes with respiratory tract disease were compared with radiographs obtained from healthy pythons. Comparisons were conducted by 2 experienced veterinarians (EWL and MCP) who were not aware of the source for each set of radiographs. Because of a poor prognosis, 3 pythons with respiratory tract disease were euthanized, and necropsies were performed.
CT assessment—All pythons were anesthetized before CT examination.17 Pythons were anesthetized by administration of diazepam (1 mg/kg, IM), followed by injection of ketamine hydrochloride (20 mg/kg, IM).
The CT examination was performed by use of a 6-slice spiral CT scanner (60-kV generator, 180-kV maximum tube voltage, and 300-mAs maximum tube current intensity).g An algorithm for soft tissue (2/6) was used for processing. The matrix was 512 X 512 pixels. Each snake was placed in a stretched position in ventral recumbency for examination, with helical scans performed after expiration and before the next inspiratory cycle. In snakes with a body length > 250 cm, 2 examinations (cranial and caudal portion) were performed to ensure complete evaluation of the lungs, including the nonfunctional part. Examinations were performed by use of the following settings: collimation, 1.5 mm; slice thickness, 2.0 mm; pitch, 0.9 with adaptation of the helix for an overlap of 0.5 mm; and tube voltage, 120 kV with adaptation of current intensity.
Lung tissues were subjectively assessed. The CT images obtained from healthy pythons and other snake species were compared with CT images obtained from the pythons with respiratory tract disease. Comparisons were performed by 2 experienced veterinarians (IK and MCP) who were not aware of the source of the CT images. Thickness, attenuation, and homogeneity of the alveolar parenchyma were assessed.
To standardize objective evaluation of morphologic characteristics and obtain information from defined areas of the lungs, a standard protocol was used. The beginning and end point of the visible alveolar parenchyma were determined. For this purpose, the consecutive axial scan series was used, and the lung tissues were subjectively assessed. The beginning was set to the first scan in which alveolar tissue was detected, whereas the end point was defined as the first scan in which no alveolar tissue was visible in the lung area (beginning of the nonrespiratory portion of the air sacs). By use of these values, length of the respiratory portion of the lungs was calculated. Three locations were then identified within the respiratory portion of each lung (locations 1, 2, and 3 at 25%, 50%, and 75% of the length of the respiratory tissue, respectively). Thickness of the alveolar lung parenchyma was measured in the axial scan along the horizontal and vertical axis through the lung at these 3 locations (Figure 1). Measurements of parenchyma attenuation were made in ROIs, which were defined as circular areas that included the entire thickness of the respiratory tissues. These ROIs were located along the horizontal and vertical axes. Therefore, cross-sectional measurements were made for the dorsal, left, right, and ventral part of each lung. In addition to these measurements, an ROI was also defined as the entire lung tissue in the same cross section, and the lung parenchyma area and attenuation were measured in this region.
Defined areas of measurement and ROIs within the lung alveolar parenchyma of a representative Indian python (Python molorus) obtained by use of an axial image during CT examination (matrix 512 X 512 pixels; window, 1,500 HUs; level,–600 HUs; 120 kV; 204 mA; and slice thickness of 2.0 mm). Thickness of the respiratory parenchyma was measured along the horizontal and vertical axes indicated, and ROIs were defined along these axes for the dorsal, left, right, and ventral part of the lung tissues (circles) in the cross-sectional image, including the entire parenchyma thickness. Additionally, an ROI was defined as the entire lung parenchyma area of the cross-sectional image. R = Right side.L=Left side. 1 = Lung parenchyma. 2 = Hypoattenuated central lumen. 3 = Muscle tissue. 4 = Vertebral column.
Citation: American Journal of Veterinary Research 68, 4; 10.2460/ajvr.68.4.428
Statistical analysis—Statistical analysis was performed by use of commercial statistical software.h All measured values were tested for a normal distribution by use of the Kolmogorov-Smirnov test. An ANOVA was conducted, or correlations with other values were tested, among relevant variables. Values of P < 0.05 were considered significant.
Measurements of attenuation in defined ROIs were made by use of internal software of the CT scanner. For each ROI, a mean value of attenuation with the associated SD for that region was determined. This SD was a variable for the distribution of attenuation within the ROI and was not the variance among samples typically associated with SD values. Therefore, SD for the ROI could be used as an indicator of homogeneity for the ROI and was treated as an independent variable (variability of attenuation).
Results
Clinical examinations—Mean ± SD body weight for the 8 healthy pythons was 11 ± 10 kg (range 2 to 34 kg), with a body length of 211 ± 67 cm (range 156 to 340 cm). Results of clinical, microbiologic, cytologic, and radiographic examination of the 8 healthy pythons were unremarkable. We did not detect pathologic findings in any of the healthy pythons.
Mean ± SD body weight for the 5 ill pythons was 20 ± 9 kg (range 12 to 32 kg), with a body length of 285 ± 61 cm (range 221 to 359 cm). Three of 5 pythons with pneumonia had severe dyspnea and massive secretion of mucus, whereas the other 2 had only mild signs of respiratory tract disease. In the 5 pythons with pneumonia, microbiologic findings revealed bacterial infection of the lungs. Main findings were gram-negative bacteria (Pseudomonas spp and Enterobacter spp). Cytologic examination revealed inflammatory cells. Parasites (hexamiths) were detected in 1 python. Radiographic examination revealed abnormal findings in the cranial portion of the lungs in 2 pythons with clinical signs of pneumonia (a mildly radiopaque area was detected in 1 python, and severe focal radiopacity was detected in the other python). Necropsy results for 3 pythons confirmed severe pneumonia with thickened lung tissues and multifocal abscesses.
CT examination—The respiratory system was evident in all 13 pythons by use of the axial plane. After multiplanar reformation, it was also evident in the dorsal and sagittal planes. The trachea and bifurcation, respiratory portion of the lungs, and caudal air sacs could be assessed (Figure 2). In 12 of 13 pythons, both lungs were visible (the left lung was not visible in 1 python). The trachea was evident as an almost-round structure, whereas the incomplete tracheal rings could not be distinguished. The lungs were visible for their entire length, with the alveolar parenchyma consistently decreasing from cranial to caudal. The caudal nonrespiratory part of the lungs was visible as an area without attenuation; its position strongly depended on the size and position of adjacent organs (Figure 3). No differences were evident for the trachea and nonrespiratory part of the lungs between healthy pythons and pythons with pneumonia.
A CT image of a representative Indian python after dorsal reformation that reveals the tracheal bifurcation and entrance of the trachea into both lungs. 1 = Trachea. 2 = Central lumen of the right lung. 3 = Alveolar parenchyma of the right lung. 4 = Central lumen of the left lung. 5 = Alveolar parenchyma of the left lung. See Figure 1 for CT variables and remainder of key.
Citation: American Journal of Veterinary Research 68, 4; 10.2460/ajvr.68.4.428
A CT image of a representative Indian python obtained by use of an axial scan that reveals the nonrespiratory part of the lungs. Structures in this area were strongly dependent on the position of adjacent organs. 1 = Vertebral column and ribs. 2 = Right air sac.3=Leftair sac. 4 = Liver. 5 = Esophagus. 6 = Aorta. See Figure 1 for CT variables and remainder of key.
Citation: American Journal of Veterinary Research 68, 4; 10.2460/ajvr.68.4.428
For the respiratory part of the lungs in healthy pythons, the alveolar parenchyma was evident as a homogeneous circular area around a hypoattenuated central lumen (Figure 4). The healthy parenchyma appeared hypoattenuated, compared with the appearance of the surrounding extrathoracic muscular tissue. The inner margin of the lung parenchyma was visible as a slightly more attenuated area. Within the parenchyma, blood vessels appeared hyperattenuated and a circular vessel plexus was evident in all healthy pythons. The margin between both sides of the lungs was visible as an area of alternating attenuation.
The CT images of a representative healthy Indian python obtained by use of an axial scan that reveals the respiratory part in the cranial (A) and caudal (B) portions of the lungs. The alveolar parenchyma is evident as an area of homogeneous attenuation with a circular vessel plexus. 1 = Right lung. 1a = Circular vessel plexus. 2 = Central lumen of the right lung.3=Left lung. 4 = Central lumen of the left lung. 5 = Vertebral column. 6 = Ribs. 7 = Aorta. 8 = Muscle tissue. 9 = Liver. 10 = Esophagus. See Figure 1 for CT variables and remainder of key.
Citation: American Journal of Veterinary Research 68, 4; 10.2460/ajvr.68.4.428
Values for lung measurements were normally distributed. Length of the respiratory part of the lungs was measured by use of information obtained during axial scanning. In all pythons in which both lungs were visible, the right lung was longer than the left lung (Table 1). A strong correlation was detected between length of the lungs and body weight (right lung, r = 0.912; left lung, r = 0.907) as well as between length of the lungs and body length (right lung, r = 0.959; left lung, r = 0.960). Therefore, for comparison of variables dependent on body size (ie, length of the lungs, area of the lung field in cross section, and thickness of lung parenchyma) between healthy pythons and pythons with pneumonia, values were reported in relation to body length.
Mean ± SD (range) measurements for CT examinations of the lungs of healthy Indian pythons (Python molurus) and pythons with respiratory tract disease.
| Pythons | Length | Mean area in cross section (mm2) | Mean thickness (mm)* | |||
|---|---|---|---|---|---|---|
| Right lung (mm) | Left lung (mm) | Location 1 | Location 2 | Location 3 | ||
| Healthy (n = 8) | 222 ± 86 (89–348) | 188 ± 69† (89–295)† | 279 ± 188 (79–594) | 5.1 ± 2.1 (2.2–9.4) | 4.2 ± 1.2 (2.2–6.0) | 2.7 ± 0.8 (2.2–5.6) |
| Ill (n = 5) | 307 ± 23 (283–336) | 244 ± 29 (205–286) | 483 ± 133 (347–675) | 6.8 ± 1.8 (2.2–6.0) | 5.0 ± 1.0 (4.0–6.0) | 2.8 ± 0.8 (3.5–6.0) |
Locations 1, 2, and 3 were at 25%, 50%, and 75% of the length of the respiratory tissue, respectively; values represent mean thickness value at each location for the dorsal, left, right, and ventral part of the lung.
Represents values for only 7 pythons.
Measurements of the thickness of the alveolar parenchyma confirmed a decrease from cranial to caudal. On average, the thickness at location 2 was 82% of the thickness at location 1, and the thickness at location 3 was 52% of the thickness at location 1.
Measurements of attenuations in the defined ROIs for the entire lung tissues of the 8 healthy pythons revealed a mean value of −746.7 HUs (mean variability of attenuation was 95.2 HUs) for the right lung and a mean value of −746.4 HUs (mean variability of attenuation was 92.2 HUs) for the left lung (Table 2). No significant differences were detected among the 3 measurement locations or between the left and right lungs. No significant differences were detected among the defined ROIs for the dorsal, left, right, and ventral part of each lung section.
Mean ± SD (range) measurements of attenuation in defined ROIs for CT examinations of healthy pythons and pythons with respiratory tract disease.
| Pythons | Entire lung tissues | Dorsal part of lungs | Left part of lung | Right part of lung | Ventral part of lungs | |||||
|---|---|---|---|---|---|---|---|---|---|---|
| Attenuation | Variability of attenuation | Attenuation | Variability of attenuation | Attenuation | Variability of attenuation | Attenuation | Variability of attenuation | Attenuation | Variability of attenuation | |
| Healthy | −744.4 ± 47.1 | 94.8 ± 9.7 | −761.0 ± 43.1 | 48.4 ± 8.0 | −756.8 ± 53.0 | 50.6 ± 18.0 | −755.4 ± 51.3 | 54.3 ± 17.0 | −761.8 ± 50.0 | 61.4 ± 6.9 |
| (n = 8)* | (−805.3 to −672.0) | (82.2 to 111.9) | (−819.1 to −693.7) | (34.8 to 63.8) | (−819.9 to −670.0) | (28.8 to 84.1) | (−831.2 to −664.0) | (28.1 to 85.7) | (−847.6 to −706.0) | (49.9 to 72.3) |
| Ill (n = 5) | −613.7 ± 176.4 | 160.9 ± 56.4 | −655.5 ± 155.0 | 99.6 ± 61.6 | −624.4 ± 173.9 | 102.0 ± 65.1 | −604.3 ± 193.1 | 121.4 ± 77.2 | −555.9 ± 214.5 | 165.3 ± 56.9 |
| (−789.0 to −359.0) | (98.9 to 226.2) | (−808.1 to −424.9) | (44.2 to 192.1) | (−770.2 to −350.1) | (39.9 to 198.1) | (−829.7 to −372.6) | (44.9 to 213.2) | (−771.8 to −266.7) | (73.3 to 211.9) | |
Represents results for 8 right lungs and 7 left lungs because only the right lung was detected in 1 python.
Clear differences were evident for the structure of the lungs in pythons with pneumonia, compared with the structure of the lungs for healthy pythons. In pythons with pneumonia, attenuation of the parenchyma appeared more nonhomogeneous with focal hyperattenuated areas. In all 3 pythons with severe signs of respiratory tract disease, the structure was nonhomogeneous for the entire extent of the respiratory tissues. The inner margin of the alveolar parenchyma (close to the central lumen) appeared thickened and hyperattenuated (Figure 5). Both pythons with moderate and mild dyspnea had alterations in the cranial part of the right lung. One python had an increase in attenuation, and nonhomogenicity was visible in the ventral area of the cross-sectional image of the lungs. In the other python, focal hyperattenuated areas were evident. In both of these pythons, the contralateral lung and the caudal parts of the left and right lungs appeared normal.
A CT image of each of 3 Indian pythons with respiratory tract disease (A, B, and C, respectively) obtained by use of an axial scan. Compared with results for healthy pythons, the alveolar parenchyma in each of these ill pythons appeared hyperattenuated and nonhomogeneous. In panels B and C, notice that only the right lung was affected. 1 = Central lumen of the right lung. 2 = Central lumen of the left lung. See Figure 1 for CT variables and remainder of key.
Citation: American Journal of Veterinary Research 68, 4; 10.2460/ajvr.68.4.428
No significant differences were detected between healthy pythons and pythons with pneumonia for length of the lungs, area of the lung field in the cross-sectional image, and thickness of lung tissue (all of which were calculated in relation to body length). A significant decrease of parenchyma thickness from cranial to caudal was confirmed for all pythons with respiratory tract disease.
For the 3 pythons with severe respiratory tract disease, measurements of the attenuations in the defined ROIs (entire lung tissues) revealed significantly higher attenuations, compared with the values for the healthy pythons (Table 2). In these 3 pythons, variability of attenuation of the lung area was significantly higher than the value for the healthy pythons. Significant differences were detected among attenuations in the dorsal (mean attenuation, −566.1 HUs; mean variability of attenuation, 134.2 HUs), middle (mean attenuation for the left and right measurements, −501.2 HUs; mean variability of attenuation, 150.9 HUs), and ventral (mean attenuation, −415.6 HUs; mean variability of attenuation, 180.4 HUs) parts of the lungs. Both attenuation and variability of attenuation within the ROIs increased from the dorsal to the ventral part of the lungs.
Analysis of measurements was conducted for the 2 pythons with mild or moderate respiratory tract disease. Analysis revealed no significant differences between values for those 2 pythons with pneumonia and values obtained for the healthy pythons (Table 2).
Discussion
Results of the clinical examinations differed in their usefulness for the diagnosis of pneumonia in the pythons in the study reported here. The microbiologic and cytologic examinations proved to be irreplaceable diagnostic aids, which indicated the type of infection and therefore provided necessary information for treatment.
However, use of radiographic examination, which has been described as the only noninvasive imaging technique suitable for diagnosis of lung alterations in larger snakes,6,16 was of limited value in our study. Of the 5 pythons with pneumonia, only 2 had radiographically detectable alterations. No correlation was detected between radiographic findings and the extent of the clinical signs. Of the 3 pythons with severe respiratory tract disease, only 1 had radiographic evidence of pneumonia. Although radiographic examination of the lungs of pythons is recommended in the literature,16 there are no guidelines regarding interpretation of the results, except for a recommendation to use radiographs of healthy snakes of the same species as a comparison. This is particularly difficult in snakes of various sizes and body weights and with varying arrangements of the internal organs.
It was possible to use CT to obtain a normal appearance of the lungs and to describe the typical parenchyma structures in the healthy pythons reported here. The protocol established for the CT examination proved to be valuable for assessment of the lungs in pythons. This protocol allowed us to assess lung tissues and obtain measurements at defined, standardized locations in lungs of these pythons independent of body length, which therefore made it possible to compare values among the snakes.
A decrease in the thickness of the respiratory tissue from cranial to caudal was confirmed. This is in accord with results of postmortem examinations of the lungs of snakes.7 Furthermore, it was possible to establish reference values for attenuation of the lung parenchyma. Remarkably, no significant difference was detected among attenuations at the various measurement areas, between the cranial and caudal part of the lungs, or between the dorsal and ventral part of the lungs. Consequently, we believe that the structure and physiologic processes of the alveolar parenchyma in healthy Indian pythons are similar for the entire length of the lungs.
In all snakes with clinical signs of pulmonary disease, alterations of the lung parenchyma that consisted of an increase in attenuation and nonhomogeneity were evident during subjective CT assessment. In pythons with severe dyspnea, these alterations were evident for the entire extent of the lungs. In contrast, they appeared more discrete and were localized only in the cranial part of the lungs in pythons with mild or moderate respiratory tract disease. It is not known whether pneumonic alterations typically develop initially in the cranial part and extend caudally in the lungs. This will need to be examined in additional studies. In the study reported here, CT examination proved to be more useful for diagnosis of pneumonia in pythons, compared with the usefulness of conventional radiographic examination, and CT examination allowed the location and extent of the alterations to be assessed.
In contrast to subjective assessment, measurements of attenuation revealed significant differences only in the 3 pythons with severe pneumonia. In these pythons, variability of attenuation within the ROIs was also significantly increased. In pythons with only mild respiratory tract disease, subjective assessment appeared to be more useful in differentiating homogeneity of the alveolar parenchyma. However, determination of attenuation may be useful for establishing a diagnosis as well as for monitoring recovery. Furthermore, assessment of attenuation revealed that in snakes with severe pneumonia, the ventral part of the lungs was significantly more affected (increased attenuation and variability of attenuation) than was the dorsal part of the lungs. Because of the constant position (ie, ventral recumbency) and saclike structure of the lungs in snakes, it is a logical consequence that inflammatory processes predominantly affect the ventral part of this organ.
During postmortem examinations, thickened alveolar parenchyma is often evident in snakes with pneumonia. In the 3 pythons that were necropsied in the study reported here, the parenchyma appeared thickened. However, the CT examination revealed that there was no significant difference intravitam between the thickness in healthy pythons and pythons with pneumonia. A possible explanation for this is that the lungs are collapsed during postmortem examinations. It is conceivable the collapse is more complete in healthy lungs with a reticular pattern that contains air, compared with the collapse for infected lungs that therefore have denser lung tissues in snakes with pneumonia. Consequently, assessment of the thickness of the alveolar parenchyma does not appear to be extremely useful for antemortem diagnosis of pneumonia in snakes.
In contrast to conventional radiography, CT revealed lung alterations in all snakes with pneumonia in the study reported here. Additionally, severity of the alterations evident during CT examinations was correlated with the extent of clinical signs. Therefore, CT examination proved to be a valuable tool for use in the diagnosis of pneumonia in Indian pythons. Additional studies in other species of snakes and clinical application in ill snakes are desirable to obtain reference data and establish CT examination as a routine diagnostic aid for use in snakes with respiratory tract disease.
ABBREVIATIONS
| CT | Computed tomography |
| ROI | Region of interest |
| HU | Hounsfield unit |
Diff-Quik, Dade-Behring, Marburg, Germany.
Columbia agar with sheep blood, Oxoid, Wesel, Germany.
Brilliant green agar (modified), Oxoid, Wesel, Germany.
Crystal tube, BD Biosciences, Heidelberg, Germany.
Sabouraud dextrose agar, Oxoid, Wesel, Germany.
Buckydiagnost AC 500, storage-phosphor-system Fuji HR 35 X 43, Philips, Hamburg, Germany.
Brilliance CT 6, Philips, Hamburg, Germany.
SPSS for Windows, version 11.5, SPSS Inc, Chicago, Ill.
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