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Evaluation of Total Lung Volume and Density using Multi-DetectorComputed Tomography in Normal Dogs

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Evaluation of Total Lung Volume and Density using Multi-Detector Computed Tomography in Normal Dogs

Ho-Jung Choi, Ki-Ja Lee*, Soo-Young Choi, Jung-Woo Lee,Woo-Sok Han**, In Lee, Young-Hang Kwon and Young-Won Lee1

College of Veterinary Medicine, Chungnam National University, Daejeon 305-764, Korea

*Department of Clinical Veterinary Science, Obihiro University of Agriculture and Veterinary Medicine, Obihiro, Hokkaido 080-8555, Japan

**College of Medicine, Konyang University, Daejeon 302-718, Korea (Accepted: Sep 19, 2011)

Abstract : This study was performed to quantitatively assess the normal lung volume and density according to the position by multi-detector computed tomography (MDCT) in dogs. Helical CT of the thorax was performed on 4 different positions with dorsal, left lateral, right lateral and ventral recumbency in 6 Pekingese and 6 Maltese dogs.

During CT scanning, dogs were kept hyperventilated. Through the 3-dimensional reconstruction of CT images, the lung parameters were measured as the volume and density of the left, right including accessory lobe, and total lung.

3D images represented the different lung shape between Pekingese and Maltese dogs. Their difference of total lung volume and total lung density was not significant on the each position in both breeds. Right lung volume was significantly higher than left. The difference of left and right volume was 66.91 ± 25.1 ml. Linear relationship was shown between body weight and lung volume of ventral recumbency position. The dependent lung had higher density and lower volume than nondependent lung in both breed dogs. The volume of nondependent lung was not changed compared with the volume on ventral or dorsal recumbency. The total lung volume measured with MDCT is correlated with the lung density, and the lung density is useful to predict the normal total lung volume.

Key words : lung volume, lung density, CT, dog.

Introduction

Lung volume is routinely assessed using pulmonary func- tion tests in human (2), but in veterinary medicine, pulmonary function test has not been used widely because of difficulty for animal’s cooperation. Pulmonary function test has a major challenge, which is the measurement of unilateral or regional lung volumes (2). Therefore, the computed tomography (CT) has been used as an imaging technique of choice for the radio- logic assessment of the thorax, and allows quantitative analysis of the lungs in human and veterinary medicine.

Several reports suggested that good correlation between helical CT-based volume calculations and the results of pulmo- nary function tests (2,8,11). Additionally, a volume acquisition of the lungs can be obtained in a single breath-hold about 20 seconds as CT technology has been advanced. Global, regional, and density-based area and volume measurements can be easily performed using CT (9,14). In especially human medicine field, three dimensional reconstruction technique has been studied for absolute lung volume and density by CT examination (2).

The extrapolation of quantitative data from human medical literature to dogs is not appropriate because of notable differ- ences in pulmonary anatomy. The previous studies in veterinary field stated that correlation of densitometric CT data with mor- phometric and histologic findings and the establishment of heli- cal CT and HRCT protocols (5), and that CT evaluation could be used to detect acute inflammatory response of lung (4).

Although several previous studies about lung CT images have been performed, normal data in lung volume and densi- ties, and the effect of breed variations have been unevaluated in dogs. The purpose of this study was performed to assess the total lung volume and density using three dimensional recon- struction technique of CT images in normal dogs, and evalu- ate the effect of body position and breed variation on the lung volume and density.

Materials and Methods

Experimental Animals

Each six of Pekingese dogs and Maltese dogs were used in this study (Table 1). The body weight was set a limit on 4 to 6 kg, in order to compare each other. Dogs without clinical signs related to respiratory system were included in this study.

Physical examination, complete blood count, serum biochemi-

1Corresponding author.

E-mail: lywon@cnu.ac.kr

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cal analysis, and thoracic radiography (four position view) were taken to evaluate healthy condition for respiratory system in the dogs. All dogs were individually housed in approved facilities within Chungnam National University

CT examination

For CT scanning, gas anesthesia was performed. All dogs were fasted for 24 hours before anesthesia. A 22G intravenous indwelling catheter was placed in a cephalic vein. The dogs were inducted with propofol (5-6 mg/kg, IV, AnepolInj®, Hana, Korea) and maintained with isoflurane (1.5 MAC, inhalation, Ifran®, Hana, Korea). The anesthetized dogs were positioned the direction of the foot-first on CT table.

CT scanning for complete thoracic cavity from sixth cervical vertebra to third lumbar vertebra level was performed on 4 positions following order as dorsal, left lateral, right lateral and ventral recumbency using MDCT (Asteion 4®, Toshiba, Japan).

Interval time for each position change was 10 minutes, and ster- nal recumbency was maintained for 10 minutes between each positions. During CT scanning, breath holding was kept with positive pressure of 15 cmH2O in order to prevent motion arti- fact by respiration. The applied technical parameters were sum- marized in Table 2.

Image processing

The image processing was performed by commercially avail- able software (Rapidia®, Infinitt, Korea). First, the obtained CT images were reconstructed to 3-dimensional (3D) of lung, the volume and density of right, left and total lung lobe were sub- sequently measured. Accessory lung lobe was included to right

lung lobe.

More precisely, the 3D reconstruction methods that was performed in this study was the following step: i) the back- ground was removed from images with 3D growing (Fig 1, B); ii) the trachea was removed using the tolerance tech- nique (Fig 1, C); iii) for subtraction of only lung, the thresh- olding technique was performed the range of between -1024 HU and -200 HU (Fig 1, D); iv) volume and density were measured with histogram of the residual voxel; v) in order to separate the left and right lung lobe, region of interest (ROI) for left or right lung was drawn, and volume and density of one side lung lobe was calculated with histogram for a selected voxels within ROI, the other lung lobe was calculated with selected voxels without ROI (Fig 2). Volumes of the lung were calculated with the voxel count method and density was used to average density of residual voxel. After image processing, lung shape of each breed was observed through 3D reconstruc- tion images (Fig 3).

Through the obtained data, it was calculated for mean total

Table 1. Signalments of experimental animals

Breed Dog (n) Body weight

Age

(year) Sex

Mean (kg)

Mean

(range) M MC F FS

Pekingese 6 5.6 5

(2-6) 0 3 3 0

Maltese 6 4.3 6.3

(3-7) 2 1 1 2

MC: male castrated, FS: female spayed Table 2. Technical parameters of CT

Parameter Value Unit

kVp 150 kVp

mAs 120 mAs

Scan thickness 2 mm

Rotation time 0.75 Rotation/sec.

Beam collimation pitch 1 Pitch

Reconstruction thickness 2 mm

Reconstruction interval 1.6 mm

Fig 1. Image processing. Through obtained image (A), the back- ground (B) and trachea (C, arrow) were removed, and only lung parenchyma is left (D).

Fig 2. ROI drawing. After image processing, ROI (yellow line) is drawn around left lung lobe in order to separate left from right lung lobe (A). Voxel counting (blue area) including ROI repre- sents the volume and density of left lung lobe (B), and voxel counting (light green area) excluding ROI represents those of right lung lobe (C).

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lung volume (TLV) and total lung density (TLD) on each breed and each position, and it was evaluated for the differ- ence of left and right lung volume and density on dependent and non-dependent position in left and right lateral positions, and relationship of body weight, density and volume.

Statistical analysis

All data were expressed as means ± SD, and 95% confi- dence interval. Comparisons among each position and each breed were performed by using one-way ANOVA test and paired t-test, respectively. Correlation of body weight to den- sity and volume were represented by Pearson’s correlation coefficient. Significant level was set at p value less than 0.05, and statistical analysis was performed by GraphPad Prism soft- ware (Graphpad Software, Inc., CA, USA).

Results

Three dimensional reconstructed images represented the dif- ferent lung shape between Pekingese and Maltese dogs (Fig 3).

In Maltese dogs, right and left lung lobe had similar shape compared to Pekingese. The cranial part of the left cranial lung lobe appeared to be wide and extend cranially and into the right cranial hemithorax in Pekingese dogs.

Total lung volumes (TLV) and densities (TLD) according to the body positions and each breed were summarized in Table 3.

TLV in Pekingese dogs was the largest relatively in dorsal Fig 3. 3D reconstruction of the lung with volume rendering tech-

nique taken by image processing. Before (A) and after (B) image processing in Pekingese dog. Before (C) and after (D) image pro- cessing in Maltese dog are shown.

Table 3. Total lung volume and density in Pekingese and maltese dogs for 4 different positions

Pekingese Maltese

Volume (ml) Density (HU) Volume (ml) Density (HU)

Dorsal 377.5 ± 74.5 −763.9 ± 39.3 304.8 ± 56.5 −729.6 ± 24.4

Lt. lateral 375.7 ± 59.2 −776.3 ± 36 286 ± 51.4 −728.3 ± 30.2

Rt. lateral 371.8 ± 65.4 −772.4 ± 38.7 269.7 ± 39.7 −716 ± 24.5

Ventral 363.1 ± 72.9 −766.1 ± 42 275.8 ± 47.2 −722.3 ± 25.7

mean ± SD (95% confidence interval) SD: standard deviation t-test: difference between Pekingese and Maltese

Fig 4. There is significant difference of body weights between Pekingese and Maltese dogs (p = 0.001).

Fig 5. The correlation of lung volume with body weight in Peking- ese (A) and Maltese (B) dogs. There is significant correlation bet- ween these parameters (R2= 0.36, p = 0.04).

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recumbency and left lateral recumbency, and TLD was the lowest in left lateral recumbency. TLV in Maltese dogs was the

largest and TLD was the lowest in dorsal recumbency. Their difference of TLV and TLD was not significant on the each position in both breeds. Generally, ventral recumbency posi- tion has been used for thoracic evaluation of CT examina- tions. Therefore, Table 4 showed total, left and right lung volume and density on ventral recumbency in all dogs. Right lung volume was significantly hihger than left. The difference of left and right volume was 66.91 ± 25.1 ml.

There was significant difference of body weights between Pekingese and Maltese dogs (Fig 4). Linear relationship was shown between body weight and lung volume of ventral recumbency position (Fig 5).

When the dogs were positioned on left or right lateral recumbency, dependent lung had higher density and lower vol- ume than nondependent lung in both breed dogs (Table 5). The volume of nondependent lung was not changed compared with the volume on ventral or dorsal recumbency.

Discussion

In this study, the quantitative measurements of total lung capacity (total lung volume at inspiratory phase) was per- formed in normal dogs using multi-detector row spiral CT. The volume and density of the lung were measured without substan- tial difficulty, and none of data was dropped out. The previous data performing the utility of CT-based measures of lung vol- ume have showed good correlation to pulmonary function test in human and dogs (2,8,11,15). In one study, the correlation of the total lung capacity with the inspiratory CT volume was higher than with the expiratory CT volume (2). This is likely due to lack of subject’s cooperation in human medicine and dif- ficulty of expiratory pause in animals. The volume of the lung Table 4. Lung volume and density of total, left lung and right lung on prone position in Pekingese and Maltese dogs

Total Lt. lung Rt. Lung

∆Rt&Lt (ml) Volume (ml) Density (HU) Volume (ml) Density (HU) Volume (ml) Density (HU)

Peki

299.787 −731.2 113.197 −726.34 183.422 −745.86 70.225

309.3 −724.82 108.29 −706.16 201.031 −734.81 92.741

299.52 −732.83 101.237 −706.5 198.307 −746.22 97.07

435.549 −824.65 180.29 −828.93 255.176 −821.77 74.886

464.67 −785.08 206.455 −791.12 258.021 −780.54 51.566

369.828 −797.73 151.663 −801.29 218.032 −795.5 66.369

Mal

243.06 −714.15 106.577 −729.8 136.459 −701.99 29.882

252.865 −738.26 104.582 −738.91 148.285 −737.8 43.703

213.027 −685.35 95.977 −709.95 117.023 −665.27 21.046

325.636 −709 119.462 −684.91 206.165 −722.99 86.703

329.652 −759.88 124.57 −756.81 205.052 −761.81 80.482

290.395 −726.96 101.07 −705.27 189.296 −738.61 88.226

Mean 319.44 −744.16 126.11 −740.50 193.02 −746.0975 66.91

SD 74.21 40.30 35.13 44.99 42.86 41.41 25.10

Peki: Pekingese, Mal: Maltese, ∆Rt & Lt: the difference of right and left lung volume

Table 5. Difference of lung volume and density expressed in percentage between dependent and non-dependent position

Difference percentage (%)

Volume Density

∆Lt. lung 20.00±10.81 5.92±3.29

∆Rt. lung 18.09±9.84 6.36±3.64

∆Lt. Lung: the difference of left lung in left and right lateral posi- tions in percentage

∆Rt. Lung: the difference of right lung in left and right lateral posi- tions in percentage

mean±SD (95% confidence interval)

Fig 6. The correlation of lung volume and density of proneposi- tion in all dogs. There are significant relationships between these parameters (R2= 0.73, p = 0.0004).

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by CT was underestimated than pulmonary function test by 12% (2) in human and by 34% in dogs (15). These results were attributed to the CT measurements’ error or lung volume decrease in supine position during the CT examination of human patients. In this study, we could not perform pulmonary function test in the dogs, so that lack of control group was the limitation. However, many reports in dogs have showed good correlation between CT and pulmonary function test, and repro- ducibility in serial quantitative CT measurements study (2,15).

For the calculation of lung volumes, three-dimensional tech- nique was applied in the present study. 3D shaded-surface dis- plays of the lungs were reconstructed with threshold of -1024 and -200. The volume of the reconstructed lungs was calcu- lated automatically. Several reports have studied about the selection of an appropriate upper threshold for the segmenta- tion of the aerated lung parenchyma (2,14). Upper thresholds of -200 or -500 HU had recommended for aerated lung volume segmentation, but lung volume have had similar correlation coefficients as compared with pulmonary function tests in the study using various upper thresholds (within range from -200 to -500 HU).

In 3D images of our study, thoracic cavity and lung shape of Pekingese dogs was different from that of Maltese dogs. It was thought that the lung shape is dependent on the shape of tho- racic cavity. It has been proposed in a previous report that the anatomy of the thorax of small, barrel-chested breeds, such as pugs, is quite different from that of large, deep-chested dogs (10). In the patient with lung lobe torsion, predisposed lung lobe has been distinct, because of the different conformation of tho- racic cavity (6,13). Further study was needed to identify between different lung shape and occurrence of lung lobe torsion.

In order to establish high resolution CT image of lung, breath holding is required during CT scanning. The positive pressure ventilation was required on breath holding is 15 cmH2O, dura- tion of < 30 seconds is considered as safe in healthy dog. There- fore, CT examination of thorax should be performed inner 30 seconds, and thin slice collimation is required to take high reso- lution image. Using MDCT with high speed of table move- ment, it is possible that CT examination of thorax was per- formed with thin slice collimation and duration of < 30 second.

2 mm slice thickness collimation of this study would be appro- priate in compared with previous study, which 4 mm thickness collimation in Beagle dogs (4,5).

In general, ventral recumbency is proper for thoracic disease on CT examinations, except for lesions close to the thoracic spine. For studies focusing on lung parenchyma, physiologic hypostatic lung collapse during anesthesia should be concerned and the position during CT examination should be dependent on the location of suspected lesion (12). In this study, the effect of position for lung volume was evaluated on four different positions; ventral, left lateral, right lateral, and dorsal recum- bency. There is no significant difference between lung volumes measured on various positions. This result was similar to the previous study performed in three Beagles (7). However, mean TLV was the largest in dorsal recumbency and the smallest in

ventral recumbency in the present study. In previous reports, lung volume was the maximum on dorsal recumbent position in human and dogs (1,7). The discrepancy between our study and previous results might be caused by duration of anesthe- sia. We performed CT scan of all dogs in order ventral, left lat- eral, right lateral and dorsal recumbency, and applied ten minute-interval time between position changes. Therefore, dor- sal recumbent scan was performed at least 30 minutes later compared with ventral recumbency.

The overall volume of the right lung is 25% larger than that of the left lung. In this study, the volume of the right lung was larger than the left in dorsal (26%) and in ventral (34%) recum- bency. These results were also similar to the previous study in which the volume of the right lung was larger than the left in dorsal (28%) and in ventral (43%) (7). They reported that the volume of the dependent lung decreased to approximately one half of that and no volume change of the nondependent lung (7). In this study, the volume of the dependent lung decreased to approximately 20% of that, and the volume of the nondepen- dent lung remained unchanged. Positive pressure inflation dur- ing anesthesia in the present study was likely to reduce the degree of change of the dependent lung volume.

TLD was negatively correlated with TLV in this study.

Lower density may represent larger lung volume in both breed dogs, TLV could be predicted by TLD on 3D reconstruction.

Total lung density in our study was higher than regional lung density in previous study, which was investigated in two bea- gle dogs (5). In one study, the density of lung changed from the apex (-800 HU) to the base (-500 HU) in twelve mixed breed dogs (3). Although that article did not present total lung den- sity, mean lung density was thought to be approximately range from -900 to -500 in normal dogs considering our results and other reports. However, mean lung density might be affected by CT equipment, protocols and status of ventilation. There- fore, ratio of lung volume or mean lung density should be con- sidered as index of lung function.

In conclusion, total or regional lung volume and density were obtained by 3D technique using helical CT at inspiration without substantial difficulties in normal dogs. Lung shape was dependent on the breed of dogs with different shape of the tho- racic cavity. Dependent lung was changed in volume and den- sity as previously described. Lung volume is respect with body weights, and negatively correlated with lung density. 3D image processing using helical CT is promising technique for diagno- sis of lung disease or research, and further studies, including pathologic examinations are needed in variable sized dogs.

Acknowledgement

This study was financially supported by research fund of Chungnam National University in 2009.

References

1. Calappi E, Mulazzi D, Cerisara M, Vercesi P, Vicardi P,

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Gattinoni L. Prone positioning improves pulmonary func- tion in obese patients during general anesthesia. Anesth Analg 1996; 83: 578-583.

2. Kauczor H, Heussel C, Fischer B, Klamm R, Mildenberger P, Thelen M. Assessment of lung volumes using helical CT at inspiration and expiration: comparison with pulmonary function tests. Am J Roentgen. 1998; 171: 1091-1095.

3. Lee HJ, Im JG, Goo JM, Kim YI, Lee MW, Ryu HG, Bahk JH, Yoo CG. Acute lung injury: effects of prone positioning on cephalocaudal distribution of lung inflation- CT assessment in dogs. 2005; 234: 151-161.

4. Morandi F, Mattoon J, Lakritz J, Turk J, Jaeger J, Wisner E. Correlation of helical and incremental high-resolution thin-section computed tomographic and histomorphometric quantitative evaluation of an acute inflammatory response of lungs in dogs. Am J Vet Res. 2004; 65: 1114-1123.

5. Morandi F, Mattoon J, Lakritz J, Turk J, Wisner E.

Correlation of helical and incremental high-resolution thin- section computed tomographic imaging with histomorpho- metric quantitative evaluation of lungs in dogs. Am J Vet Res. 2003; 64: 935-944.

6. Neath P, Brockman D, King LG. Lung lobe torsion in dogs: 22 cases (1981-1999). J Am Med Assoc. 2000;

217: 1041-1044.

7. Nils-Eriakhlberg A, Hoppe F, Kelter U, Svensson L. A computed tomographic study of volume and X-ray att- enuation of the lungs of beagles in various body posi- tions. 1985; 26: 43-47.

8. Patroniti N, Bellani G, manfio A, Maggioni E, Giuffrida

A, Foti G, Pesenti A. Lung volume in mechanically ventilated patients: measurement by simplified helium dilu- tion compared to quantitative CT scan. Intensive care medicine. 2004; 30: 282-289.

9. Puybasset L, Cluzel P, Chao N, Slutsky AS, Corat P, Rouby JJ. A computed tomography scan assessment of regional lung volume in acute lung injury. Am J Resp Crit Care Med. 1998; 158: 1644-1655.

10. Rooney MB, Lanz O, Monnet E. spontaneous lung lobe torsion in two pugs. J Am Anim Hosp Assoc. 2001;

37: 128-130.

11. Schlesinger AE, White DK, Mallory GB, Hildeboldt CF, Huddlesoton CB. Estimation of total lung capacity from chest radiography and chest CT in children: comparison with body plethysmography. Am J Roentgenol. 1995;

165: 151-154.

12. Schwarz T. Basics of thoracic computed tomography. In:

BSAVA manual of canine and feline thoracic imaging, 1st ed. Gloucester. 2008: 66-70.

13. Seiler G, Schwarz T, Vignoli M, Rodriguez D. computed tomographic features of lung lobe torsion. Vet Radiol ultrasound. 2008; 49: 504-508.

14. Simon BA, Christensen G, Low D, Reinhardt J. Com- puted tomography studies of lung mechanics. Proceedings of the American Thoracic Society. 2005; 2: 517-521.

15. Wandtke JC, Hyde RW, Fahey PJ, Utell MJ, Plewes DB, Goske MJ, Fischer HW. Measurement of lung gas volume and regional density by computed tomography in dogs. Invest Radiol. 1986; 21: 108-117.

정상견에서 다중채널 컴퓨터단층촬영술을 통한 폐용적과 밀도의 평가

최호정·이기자*·최수영·이정우·한우석**·이인·권영항·이영원1

충남대학교 수의과대학, *오비히로 농과대학 임상수의학부, **건양대학교 의과대학

요 약 : 개에서 컴퓨터단층촬영술을 이용하여, 촬영 자세에 따른 정상 폐의 용적과 밀도를 정량적으로 평가하였다. 각 각 6 마리의 페키니즈견과 말티즈견에서 컴퓨터단층촬영을 실시하면서 자세를 앙와위, 좌측과 우측 횡와위, 그리고 흉 와위로 변경하였다. 컴퓨터단층촬영을 실시하는 동안 일정한 정도의 양압환기를 실시하였다. 폐용적과 밀도는 CT 영상 의 삼차원 재구성 방식을 통해 측정하였고, 전체 폐용적 및 밀도, 좌측과 우측 폐의 용적과 밀도를 각각 측정하였다.

삼차원 재구성 결과 폐의 모양은 두 품종견에서 매우 다르게 나타났다. 폐용적과 밀도는 촬영 자세를 변경하는 동안 두 품종견에서 모두 유의적인 변화를 보이지 않았다. 오른쪽 폐용적이 왼쪽 폐에 비해 유의적으로 약 66.91±25.1 ml 만큼 컸다. 페키니즈 견과 말티즈 견의 체중 차이가 유의적이었으며, 체중과 흉와위로 촬영한 폐용적 간에 선형관계가 관찰되었다. 좌우측 횡와위 촬영에서 중력의 영향을 받는 쪽의 폐는 반대쪽 폐에 비해 밀도는 높고 용적은 감소되었 다. 컴퓨터단층촬영으로 측정한 전체 폐용적은 폐밀도와 관련이 있었으며, 폐밀도가 정상 폐용적을 유추하는데 유용하 게 사용될 것으로 생각된다.

주요어 : 폐용적, 폐밀도, 컴퓨터단층촬영, 개

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