The diaphragm is the principal muscle used in respiration. Excursion of the diaphragm is driven by the phrenic nerve. Diaphragmatic contraction causes expansion of the thoracic cavity, which results in lung inflation in a craniocaudal direction.1–3 The range of diaphragmatic movement is directly related to the inspiratory volume.
Unilateral or bilateral diaphragmatic paralysis is caused by insufficiency of the phrenic nerve in adverse neuromuscular conditions (eg, trauma, compression or degeneration of the phrenic nerve, and myopathy) and other conditions (eg, pneumonia and idiopathic conditions).4–8 Unilateral diaphragmatic paralysis is often not associated with clinical signs and only observed incidentally or may manifest as orthopnea or dyspnea during exertion. Bilateral impairment is usually not associated with clinical signs, which results in ventilatory failure, followed by cyanosis with apnea.4,7,9–12
Various imaging modalities have been proposed for use in the evaluation of diaphragmatic excursion. For radiographic evaluation of dogs, the dependent crus in lateral radiographs typically is cranial to the contralateral crus, and asymmetry between the crura may represent normal variation, except that 1 crus is consistently located cranial to the other crus, regardless of positional changes.13,14 In addition to the confusion caused by these imaging variations, detection and characterization of diaphragmatic dysfunction are unreliable when using conventional radiography because of variations in the x-ray beam center, respiration, and gastric pressure and the posture, size, breed, age, and obesity of the patient.5,14 Therefore, a dynamic imaging technique is essential for precise diagnosis of diaphragmatic paralysis.
Fluoroscopy and ultrasonography are currently the diagnostic tools of choice for such a diagnosis.7 Ultrasonography is a good modality for subjective evaluation of diaphragmatic movement, but it does not allow simultaneous visualization of both the right and left sides of the diaphragm. Fluoroscopy allows observation of diaphragmatic excursion during breathing in real time as well as simultaneous examination of the right and left sides of the diaphragm. Inherent characteristics of fluoroscopy allow qualitative assessment of diaphragmatic motility as well as quantitative measurement of excursion.5,15 In fluoroscopic images of the diaphragm of humans, both the right and left parts of the diaphragm move caudally as the anterior chest wall moves upward during respiration.16 Unequal movement between the diaphragmatic crura has been suggested to indicate unilateral paralysis. It may be more difficult to confirm bilateral paralysis with fluoroscopy when compensatory abdominal muscle contractions cause diaphragmatic movement. Nevertheless, minimal or absent diaphragmatic movement or a paradoxical cranial displacement of a flaccid diaphragm may be observed during inspiration in patients with diaphragmatic paralysis.11
Fluoroscopic diagnosis of diaphragmatic paralysis has been reported in only a few dogs, including 1 dog with unilateral paralysis10 and 2 dogs with bilateral paralysis.10,11 Radiographically, the dog with unilateral paralysis had cranial displacement of the left crus relative to the right crus, which was separated by a gap corresponding to the length of 2 vertebrae. Unequal movement was observed fluoroscopically, and the left crus had minimal movement, with an amplitude of less than one-half of an intercostal space. For the 2 dogs with bilateral paralysis, no diaphragmatic movement was detected radiographically, although cranial displacement of both crura was observed radiographically and paradoxical cranial motion of a flaccid diaphragm during inspiration was observed fluoroscopically. For these dogs, fluoroscopic diagnosis of diaphragmatic paralysis was based on subjective determination of diaphragmatic motion during respiration. Quantitative data on diaphragmatic motion, particularly crural excursion, on the basis of the phase of respiration and dog's position may facilitate detection of abnormal diaphragmatic motion. Quantitative data on diaphragmatic movement in humans measured fluoroscopically have been reported.5,15,17–19
The purpose of the study reported here was to quantitatively evaluate diaphragmatic movement in clinically normal Beagles by use of fluoroscopy. The hypotheses were that excursion would differ among parts of the diaphragm during physiologic respiration and that excursion for the various parts of the diaphragm would be affected by the position of each dog during respiration.
Materials and Methods
Animals
Eight male Beagles were used in the study. Dogs were 2 to 3 years old, and mean ± SD body weight was 10.46 ± 0.76 kg (range, 9.6 to 11.4 kg). No previous or current signs of respiratory tract disease were identified in any of the dogs. All dogs were considered healthy on the basis that no abnormalities were detected during physical examination and results of a CBC, serum biochemical analysis, electrolyte tests, and urinalysis were within reference limits. Right lateral and ventrodorsal thoracic radiographs were obtained with a digital radiographic systema; dogs were not sedated or anesthetized for radiography. Radiographs were examined to verify that there were no respiratory tract abnormalities. Dogs were cared for in accordance with guidelines for the Laboratory Animal Research Center, and all experiments were approved by the Institutional Animal Care and Use Committee at Chonnam National University (CNU IACUC-YB-2014-14).
Fluoroscopic examination
Food was withheld from all dogs for at least 12 hours to reduce gastric effects on the diaphragm, and dogs were kept in a quiet room to allow respiration to stabilize. The beam center was located at the level of the diaphragm, and the field was set at 27 × 27 cm for fluoroscopic examination.b Diaphragmatic movement was recorded (speed of 32 frames/s) by use of integrated recording softwarec during 3 respiratory cycles with dogs positioned in left lateral, right lateral, and dorsal recumbency. Recordings were then transferred to a picture-archiving and communication system.d
Image analysis
Diaphragmatic excursions were measured separately by 2 radiologists (SM and SP) by means of electronic calipers. For the 3 cycles of each position, the one with the most harmonious movement without sudden movements, reflex movements, or vocalization of the dog was selected for analysis. Two still images that included the extreme cranial and caudal locations of each diaphragmatic part during respiration were selected for analysis. The shortest distances from the centers of the left and right crura and the diaphragmatic cupula at the most cranial diaphragmatic location to the corresponding parts at the most caudal location were defined as the excursions of these parts (Figure 1). Excursions of the 3 diaphragmatic parts and the length of the body of T8 were obtained, and ratios of the excursion of each diaphragmatic part to the length of the body of T8 were calculated. In addition, the difference between excursions of the right and left crus was measured to assess asymmetric movement of each crural position and was expressed as a percentage of the excursion of the diaphragmatic part with the least movement.20 Asymmetric motion was defined when there was a significant difference in mean excursion between the left and right diaphragmatic crura.
Schematic drawing indicating measurement of the excursion of the left crus (L), right crus (R), and diaphragmatic cupula (B) for a dog positioned in right lateral recumbency for fluoroscopic examination. The center of each diaphragmatic part during expiration is indicated (arrowheads). Excursion is defined as the shortest distance between the expiratory and inspiratory position of each part of the diaphragm (double-headed arrows).
Citation: American Journal of Veterinary Research 78, 9; 10.2460/ajvr.78.9.1043
Statistical analysis
Values were expressed as mean ± SD. The maximum and minimum excursion of the diaphragm and ratio of the excursion to the length of the body of T8 were also reported. Differences among recumbency positions and diaphragmatic parts were evaluated by use of the Kruskal–Wallis test and Whitney signed rank test with a Bonferroni correction for multiple comparisons. Interobserver reproducibility was determined by calculating the ICC. Interpretation of the cutoff range for ICC was as follows: ≤ 0.40, poor agreement; 0.41 to 0.60, moderate agreement; 0.61 to 0.79, good agreement; and ≥ 0.80, excellent agreement.21 For all tests, differences between 2 groups were considered significant at P < 0.05. The value for α was adjusted to 0.0167 by use of a Bonferroni correction for multiple tests for comparisons within the recumbency positions and diaphragmatic parts. Analyses were performed with statistical software.e
Results
A total of 24 fluoroscopic images were obtained for the 8 Beagles. Diaphragmatic excursions were easily observed during respiration and were successfully assessed in all fluoroscopic images. Physiologic diaphragmatic excursion occurred in a cranial or caudal direction, opposite to the caudal or cranial movement, respectively, of the thoracic wall. The 2 sides of the diaphragm moved together, and no paradoxical movement was observed in any of the dogs.
The excursion of each diaphragmatic part was not significantly different among the dogs for each bency position. Movement of the right crus was significantly less for dorsal recumbency than for the other recumbency positions. Mean excursions of the left crus and diaphragmatic cupula were not significantly different among recumbency positions. Mean excursions of the left and right crura were not significantly different for right lateral recumbency; however, mean excursion among diaphragmatic parts was significantly different for left lateral and dorsal recumbency (Table 1). Mean excursion was asymmetric for the left lateral and dorsal recumbencies, with greater excursion for the left crus than the right crus. Mean ± SD difference in excursion between the crura was 22.68 ± 8.68% (range, 5.68% to 35.96%) for left lateral recumbency, 16.63 ± 9.22 % (range, 1.70% to 35.41%) for right lateral recumbency, and 18.11 ± 12.96% (range, 2.57% to 38.02%) for dorsal recumbency.
Results of fluoroscopic measurement of the excursion of each diaphragmatic part in dogs positioned in right lateral, left lateral, and dorsal recumbency.
| Right lateral recumbency | Left lateral recumbency | Dorsal recumbency | ||||
|---|---|---|---|---|---|---|
| Part | Mean ± SD | Range | Mean ± SD | Range | Mean ± SD | Range |
| Cupula | 11.14 ± 1.93a | 8.06–14.43 | 10.68 ± 3.14a | 5.88–15.85 | 9.30 ± 3.23a | 2.35–14.29 |
| Right crus | 13.48 ± 2.06b | 11.26–17.99 | 13.65 ± 4.81b | 6.78–21.81 | 10.91 ± 1.46b | 8.51–13.23 |
| Left crus | 13.51 ± 3.38b | 8.94–20.25 | 15.72 ± 7.21c | 5.48–32.31 | 13.05 ± 2.06c | 9.41–17.77 |
Values reported are number of millimeters and represent results for 8 healthy Beagles.
Within a column, values with different superscript letters differ significantly (P < 0.05).
Ratios of the excursions of the right and left crura to the length of the body of T8 measured for left lateral recumbency differed significantly among the dogs. However, the ratio of the excursion of the cupula of the diaphragm to the length of the body of T8 for left lateral recumbency and the ratios of the excursion of each diaphragmatic part to the length of the body of T8 for the right lateral and dorsal recumbencies did not differ significantly among the dogs. Mean ratio of the excursion to the length of the body of T8 was significantly different among the diaphragmatic parts for each recumbency (Table 2). However, mean ratio of the excursion to the length of the body of T8 did not differ significantly between the left and right crura for right lateral recumbency; mean ± SD value of the ratios of both crura was 0.73 ± 0.13 (range, 0.52 to 1.05). Mean ratio of the excursion of the right crus to the length of the body of T8 differed significantly according to recumbency position; mean excursion of this diaphragmatic part for dorsal recumbency was smaller than those for the other recumbency positions. Mean ratios of the left crus and diaphragmatic cupula did not differ significantly among recumbency positions.
Ratio of the excursion of each diaphragmatic part to the length of the body of T8 for the dogs in Table 1.
| Right lateral recumbency | Left lateral recumbency | Dorsal recumbency | ||||
|---|---|---|---|---|---|---|
| Part | Mean ± SD | Range | Mean ± SD | Range | Mean ± SD | Range |
| Cupula | 0.60 ± 0.10a | 0.47–0.82 | 0.58 ± 0.18a | 0.30–0.86 | 0.49 ± 0.19a | 0.12–0.85 |
| Right crus | 0.73 ± 0.10b | 0.61–0.93 | 0.74 ± 0.26b | 0.35–1.12 | 0.57 ± 0.09b | 0.39–0.70 |
| Left crus | 0.73 ± 0.16b | 0.52–1.05 | 0.85 ± 0.36c | 0.29–1.59 | 0.69 ± 0.12c | 0.48–0.91 |
Values represent results for 8 dogs.
See Table 1 for remainder of key.
Interobserver reproducibility was excellent. Mean ICC was 0.913 (range, 0.775 to 0.980) for the excursion measurements, except for excursion of the right crus for right lateral recumbency (ICC, 0.775) and for length of the body of T8 (ICC, 0.906; range, 0.864 to 0.979).
Discussion
For the study reported here, dynamic movement of the diaphragm was evaluated by use of fluoroscopy, and quantitative data for diaphragmatic excursion in clinically normal dogs during spontaneous breathing were reported. Fluoroscopy allowed the investigators to perform real-time evaluation of motion of the entire diaphragm as well as to obtain qualitative measurements.
Fluoroscopy has been used to identify diaphragmatic paralysis on the basis of visual assessment of motion.10,11 However, characteristics of physiologic movement of the diaphragm have not been evaluated by use of fluoroscopy; in particular, the influence of a dog's position has not been evaluated fluoroscopically. Human diaphragmatic excursion has been quantitatively assessed by use of only the caudal-cranial view for the erect position, and vertical excursion has been measured parallel to the thoracic vertebra.15,17–19 In the present study, diaphragmatic excursion was measured as the shortest distance between locations from inspiration to expiration for right and left lateral recumbency to reflect the oblique movement of the diaphragm in each of the positions.14 In the present study, the diaphragmatic crura had different movement patterns on the basis of the lateral recumbency position. The right and left crura had similar movements for right lateral recumbency; however, asymmetric movement of the diaphragm was greatest for left lateral recumbency, with the left crus having greater excursion than the right crus. Unilateral paralysis of the diaphragmatic crus may need to be evaluated in dogs in right lateral recumbency to reduce confusion.
Diaphragm movement in humans with diaphragmatic paralysis has been quantitatively analyzed. Quantitative analysis of diaphragmatic excursion can be used to complement visual analysis of fluoroscopic images. Quantitative analysis in the present study revealed that diaphragmatic excursion of the crura differed during respiration from 50% of the length of the body of T8 to the full length of the body of T8 (mean value, 75% of the length of the body of T8) for right lateral recumbency. Dorsal recumbency resulted in different excursion patterns between the 2 crura; excursions differed from 40% to 70% and from 50% to 90% of the length of the body of T8 for the right and left crus, respectively. Unequal excursion between the left and right crura was significantly different for left lateral recumbency (mean value, 23% of the length of the body of T8), with a value < 40% of the length of the body of T8 for every recumbency position.
Diaphragmatic excursion has been investigated in a large number of clinically normal humans. Mean excursions of the domes of the right and left sides of the diaphragm were 3.3 and 3.5 cm, respectively, whereas excursion typically was slightly asymmetric, with a slight delay or lag on 1 side (typically the right side).20,22
Characteristics of physiologic diaphragmatic excursion in the present study were similar to those of previous reports,20,22 although humans and dogs differ with regard to thoracic conformation. Irrespective of the lateral recumbency in which a dog was placed in the present study, the lower portion of the diaphragm sagged and moved cranially because of the effect of gravity on the abdominal viscera.14 However, recumbency position did not have a significant effect on excursions. Although the left crus had amplitude similar to that of the right crus for right lateral recumbency, the left crus moved more than did the right crus for left lateral recumbency, which resulted in asymmetric movement of the crura in either lateral recumbency. Therefore, assessment of radiographic views for dogs in left lateral recumbency may be more sensitive for detection of diaphragmatic paralysis and has the best negative predictive value, whereas assessment of radiographic views for dogs in right lateral recumbency may be most specific and have the best positive predictive value.
The left crus usually had greater excursion than the right crus, which is consistent with data for humans.20,22,23 In contrast, in another study,18 changing the side of lateral recumbency (ie, positioned on the opposite side) resulted in increased amplitude of the uppermost crus, which is in contrast to findings for the study reported here. These conflicting results could be explained by the fact that the difference was not significant in the previous study,18 and humans and dogs have numerous differences in terms of thoracic composition and the position and shape of visceral organs.
The reason that amplitude of the right crus significantly decreased when the position was changed from lateral recumbency to dorsal recumbency is not clear. This finding may be explained by an inherent characteristic of the right crus. The excursion of each crus was not measured in separate cycles in the present study; therefore, excursion of the lagging part of the diaphragm (the right crus) may have been underestimated, although we did not notice lagging of the right crus during visual observation. In addition, magnification of each crus should be considered when obtaining diaphragmatic measurements for dogs in lateral recumbency. However, magnification was not considered to be a major factor affecting diaphragmatic measurements for dogs in lateral recumbency because symmetry and excursion of right and left diaphragmatic crura differed on the basis of left or right lateral recumbency, although the distance from the uppermost crus to the image detector was the same for each lateral recumbency.
Fluoroscopy requires precise positioning of subjects and use of ionizing radiation. In studies of humans, fluoroscopy can be used to detect > 90% of unilateral diaphragmatic abnormalities; however, the test is not as useful for diagnosing bilateral diaphragmatic paralysis. False-positive results are evident in 6% of patients who do not have diaphragmatic paralysis.20
Measurements for the study reported here were obtained during stabilized respiratory conditions, whereas sick dogs are usually more prone to panting or hyperventilation. Excursion decreases with panting and increases with hyperventilation.14 Although it is uncertain whether results obtained for the present study would be applicable to unhealthy subjects, the direction of excursion may be a helpful criterion for detecting paralysis.22 The method for measuring excursion used in the present study has not been proven to be more effective or reliable than the method used previously for humans, whereby excursion is measured parallel to the vertebrae. Comparative studies with pneumotachography or respiratory inductive plethysmography should be performed to investigate the method that most accurately reflects excursion or ventilation.
Other limitations of the study reported here were the small sample size and the use of dogs of only 1 breed. Additional studies with larger sample sizes and various breeds of clinically normal as well as unhealthy dogs should be performed. Moreover, clinically normal status of dogs of the present study was not confirmed by use of pulmonary function tests (eg, pneumotachography or respiratory inductive plethysmography). Although thoracic radiography was used to identify that there were no respiratory tract abnormalities, some dogs with subclinical respiratory diseases may have been included in the present study.
Data on excursion of the diaphragm in clinically normal Beagles evaluated by use of fluoroscopy were reported in the present study. Analysis of these data indicated that excursion appeared to be most asymmetric for dogs in left lateral recumbency and relatively symmetric for dogs in right lateral recumbency, with a crural excursion of approximately 75% of the length of the body of T8. This information should be considered so that false diagnoses of diaphragmatic paralysis can be minimized when dogs are positioned in left lateral recumbency. Furthermore, evaluating asymmetry of dogs in right lateral recumbency may result in a higher sensitivity for detection of unilateral paralysis than for other recumbency positions.
Acknowledgments
Supported by the Basic Science Research Program through the National Research Foundation of Korea (NRF), funded by the Ministry of Science, Information and Communication Technology, and Future Planning (grant No. 2015R1A2A2A01003313).
ABBREVIATIONS
| ICC | Intraclass correlation coefficient |
Footnotes
PcCR1417, OREX Computed Radiography Ltd, Yokneam, Israel.
KMC-950, Gemss-Medical, Seoul, Republic of Korea.
CXView, version 3910, Gemss-Medical, Seoul, Republic of Korea.
INFINITT, Infinitt Healthcare, Seoul, Republic of Korea.
SPSS for Windows, release 21.0, SPSS Inc, Chicago, Ill.
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