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For these reasons, we chose to investigate the pig as a model for RILI. The methods for in vivo lung procedures in the pig have rarely been described. Some groups have used breathing rates to assess pneumonitis [ 30 ], but had limited success in monitoring fibrosis. Some groups have measured cytokine and growth factor expression induced in the lung after irradiation [ 31 , 32 ], although none of the cytokines or growth factors evaluated have been shown to directly cause lung injury.
Chest computed tomography CT has been introduced as a radiological diagnostic method for detecting lung abnormalities [ 33 ]. It is safe, non-invasive and widely accessible, making it well suited for clinical implementation, and its distinct patterns for lung injury have been previously described from the lungs of humans receiving radiotherapy [ 34 ]. Some groups have used CT previously [ 35 , 36 ], but limitations of studies to date include largely qualitative radiologic interpretation, diagnostic variability among observers, and the necessity for specialized expertise [ 37—40 ].
For the objective quantitative analysis of lung injury progression by thoracic CT, measurement of Hounsfield units HU and 3D reconstruction from thoracic CT sections have been used to assess the changes in lung density and volume, respectively. However, in the case of 3D reconstruction of the lungs, processing requires multiple steps, is time-consuming [ 41—43 ], and other than HU measurement, lacks easily quantifiable parameters.
The goal of the current study was to describe the use of an optimal minipig model for assessing RILI induced by a single high-dose radiation exposure, and to evaluate RILI progression via a thoracic CT technique employing novel quantitative parameters. Prior to purchase, the pigs were physically examined and determined to be healthy. Pigs were housed indoors in individual cases, fed dry pig food and provided with triple-filtered water.
Precise localization of whole right lung lobes for determining irradiation fields was performed under chest X-ray guidance SMHF, Listem, Seoul, Korea.
For irradiation, the minipigs were placed in the prone position and irradiated in a 60 Co gamma-ray irradiation unit Theratron , AECL, Ontario, Canada ; the average calculated dose rate at the center of the field was The distance between the source of radiation and the thoracic skin was 80 cm. After irradiation, pigs were housed individually, fed dry pig food and provided with triple-filtered water under environmentally controlled conditions.
Briefly, thoracic CT scanning was performed using a multi-detector-row CT unit Asteion Super 4; Toshiba, Tokyo, Japan with the following parameters: tube voltage, kVp; tube current, 12 mAs; and slice thickness, 3 mm. The 2D CT cross-sections and subsequently reconstructed 3D images of the lungs were obtained using a 3D imaging software Rapidia; Infinitt, Seoul, Korea , and CT cross-sections were displayed in the lung window window width, ; window level, — For all CT procedures, the pigs were under general anesthesia and placed in the prone position on the CT table.
Ltd, Seoul, Korea and maintained by 1. All CT images were acquired during a single breath-hold. The CT scans were interpreted by two expert radiologists from the Ian Animal Diagnostic Imaging Center who were blinded to the experimental groups. All endoscopic evaluations were performed under anesthesia. Endoscopic examination of the irradiated bronchus using fiber-optic endoscopy Pentax EG K, Japan was performed at 6 weeks and 12 weeks after irradiation.
Gross changes were evaluated by independent endoscopists. Sterile normal saline 10 ml was instilled into the lungs, and then the fluid was aspirated into a sterile container. The cells in the bronchoalveolar lavage fluid BALF were counted using a hemacytometer. At 22 weeks after irradiation, minipigs were anesthetized, euthanized and necropsied. The extent of pulmonary fibrosis was quantified using a modified Ashcroft histopathology scoring system [ 45 ].
A paired t -test was used to determine statistically significant differences in outcomes before and after irradiation. Regression analyses were used to assess the association between fibrosis score and the three quantified CT parameters. A P value less than 0. Due to the exploratory nature of this study, P -values were reported without multiplicity adjustments.
Thoracic CT findings after irradiation revealed increased intensities in peribronchial areas and thickening of the interlobular septa and the peribronchial region. Increased opacities and volume loss of irradiated lung lobes were also seen on CT sections Fig. Time-course evaluation of thoracic computed tomography CT in control, and 25 and 30 Gy irradiation groups. A Representative images of thoracic CT scans of non-irradiated and irradiated lungs.
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Note thickening of the interlobular septa and peribronchial regions, increased parenchymal opacifications, and architectural distortion of lung lobes in irradiated right lungs along with cardiac right lateral shift. Arrows indicate lung volume loss in non-irradiated or irradiated lungs reconstructed from thoracic CT scans. B Quantitative data obtained from thoracic CT scans regarding HU value left , lung area ratio middle , and cardiac right lateral shift right. Hemi-thoracic irradiation to the lungs induced significant changes in the three quantitative CT parameters.
HU values peaked at 6 weeks, and lung area steadily decreased in a time-dependent manner; cardiac right lateral shift was significantly increased after 17 weeks. Cardiac right lateral shift was evaluated to determine the degree of anatomical deviation of the heart and lung resulting from radiation-induced injury.
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We assessed the time-course of the cardiac right lateral shift at 6, 12, 17 and 22 weeks after irradiation Fig. Furthermore, to explore a potential time relationship between HU values and WBC counts or LDH levels, the correlation was examined at the 6, 12, 17 and 22 week time-points after irradiation. Time-course evaluation of pneumonitis in control and irradiation groups.
A WBC counts peaked at 6 weeks and decreased after 17 weeks. C Plasma LDH peaked at from 6—12 weeks and decreased after 17 weeks. Bronchoscopic examination was performed to evaluate inflammation and irregularities of the lungs at 6 and 12 weeks post irradiation. We confirmed normal bronchial trees in the irradiated lungs by CT Fig.
Bronchoscopic evaluation of pneumonitis at 6 and 12 weeks in 30 Gy-irradiated animals.
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The irradiated lung lobe showed consolidation, although normal bronchial trees were observed. B Gross evaluation by bronchoscopy. The irradiated lung did not show any gross lesions upon bronchoscopic evaluation. In control lungs, collagen was present in the interlobular septa, and the lobularity was well developed. However, in the irradiated lungs, thickened alveolar walls and widening of the interlobular septa with fibrotic changes were observed Fig. Dense fibrosis was noted, mainly in the interlobular septum rather than in the interstitium of the alveolar space, and was more prominent in the Gy—irradiated lungs than in the Gy—irradiated lungs.
Moreover, modified Ashcroft scores were significantly increased in the irradiated right lungs of the 25 and 30 Gy groups compared with the control group Fig. Histopathologic evaluation of right lung lobe tissues in control, 25 Gy, and 30 Gy groups at 22 weeks post irradiation. Note that the thickening of interlobular septa with collagenous tissue arrows was more severe in the 30 Gy group than in the 25 Gy group. Scale bar represents 1 mm right bottom. B Quantitative fibrosis scores of non-irradiated and irradiated right lungs using the modified Ashcroft fibrosis scoring system.
Hemi-thoracic irradiation increased fibrosis grade in a dose-dependent manner. Thoracic CT findings at 22 weeks after irradiation revealed characteristics of lung fibrosis Fig. Lungs exposed to 30 Gy showed homogeneously increased opacities in the right upper lobes, which were sharply demarcated from the other lobes.
Volume loss of the right lung lobes was also confirmed by 3D reconstructed images of the lungs Fig. The cardiac right lateral shift was significantly increased in irradiated animals 22 weeks after irradiation Fig. Thoracic computed tomography CT of non-irradiated or irradiated lungs in control, 25 Gy, and 30 Gy groups at 22 weeks post irradiation IR. A Quantitative data obtained from thoracic CT scans regarding HU value left , lung area ratio middle and cardiac right lateral shift right.
Hemi-thoracic irradiation to the lungs induced dose-dependent changes in three quantitative CT parameters. B Correlation analysis of quantitative CT parameters to histological fibrosis score. Three quantified CT parameters HU value, lung area and cardiac right lateral shift were strongly and significantly correlated to modified Ashcroft fibrosis scores the Spearman's correlation coefficients were 0.
The modified Ashcroft fibrosis scores and quantitative CT parameters at 22 weeks post irradiation were plotted to explore a potential correlation. The minipig is emerging as an alternative large animal model for characterizing acute radiation syndrome ARS [ 3 , 33 , 34 ], and we are evaluating the minipig as an RILI model.
Animal models should show similarities in lung radiation dose responses and time-courses to those seen in humans [ 1 ]. The radiation doses for RILI in rats were in the range of 10—15 Gy to the whole thorax or 25—28 Gy to the hemithorax [ 46—48 ]. In order to investigate dose responses and time-courses for the development of pneumonitis and fibrosis, we designed a strategy for irradiating the right hemithorax rather than the whole thorax, which was expected to reduce mortality, thereby allowing a long-term study of the development of lung fibrosis in the late phase, and permitting each animal to act as its own control [ 7 ].
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Most of the spectra of changes seen on thoracic CT of radiotherapy-induced fibrosis in human lungs were also identified in our minipig model. However, the radiological interpretation of the CT findings in humans was limited, because the findings were largely qualitative and needed refinement.
Thus, we measured numerical values easily obtainable from CT images to allow more rapid, quantitative assessment of RILI. The first parameter that we used was the HU value. The HU value reflects lung density and has been investigated by several groups using chest CT [ 33 , 50—52 ].
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The second parameter was the lung area ratio of the transverse CT section. The lung area ratio was determined from measurements of four regions as described in the Materials and Methods, and is thought to reflect changes in the size of the lung lobes induced by the various radiation doses. The last CT parameter that we adapted was the degree of cardiac right lateral shift.
The heart is the largest mediastinal organ, and a decrease in lung volume due to lung fibrosis results in its anatomical deviation toward the affected lung [ 53 , 54 ]. To confirm the presence of pneumonitis, we used clinical diagnostic methods, including: complete blood count, bronchoscopy, and BALF cytology.
BALF cytology also showed an increase in the number of WBCs, neutrophils and lymphocytes at 6 and 12 weeks post irradiation. However, we did not observe any inflammation or irregularities in the bronchial trees upon bronchoscopic evaluation. To confirm fibrosis-related findings by CT, histopathological analysis was performed. The most characteristic histological feature of fibrosis observed was thickening of the interlobular septa with dense collagenous tissue.
Our histological findings regarding lung fibrosis in the minipigs were in agreement with those of other investigators, who have demonstrated interlobular septal thickening induced by irradiation in swine lungs [ 7 , 36 , 55 ]. The heterogeneous distribution of thickened alveolar walls, further restricted by widening of the interlobular septa due to dense fibrosis, would render the alveoli unable to function normally; this distinctive pattern of fibrosis may explain the greater radiosensitivity observed in the lungs of pigs, and indeed humans, as compared with rodents after a single high-dose exposure to radiation [ 7 ].
Lastly, we demonstrated strong and significant correlations between the histological fibrosis scores measured by the modified Ashcroft scoring system and our CT parameters. A major strength of our minipig model and experimental design is that it allows the same animal to serve as both a test and a control subject.
Furthermore, by using our three chest CT parameters, investigators can obtain quantifiable clinical data by simple translation methods. As we seek treatment strategies for radiation-induced lung fibrosis, this objective, quantitative technique using chest CT could emerge as a valuable tool for pre-clinical studies. The authors would like to thank the Ian Animal Diagnostic Imaging Center, Korea, for support in thoracic CT image acquisition and radiological interpretation.
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