Animal models of smoke inhalation injury and related acute and chronic lung diseases

Advanced Drug Delivery Reviews

Volumn 123, Issue , 2018, Pages 107-134

  Reczyńska, Katarzyna ^a,b   Tharkar, Priyanka ^b   Kim, Sally Yunsun ^b   Wang, Yiwei ^b   Pamuła, Elżbieta ^a   Chan, Hak Kim ^b   Chrzanowski, Wojciech ^b  

^a AGH UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Poland)

^b UNIVERSITY OF SYDNEY   (Australia)

Author keywords

Large animals; Lung injury models; Small animals; Smoke inhalation

Indexed keywords

BIOLOGICAL ORGANS; PATHOLOGY; SMOKE;

CHRONIC LUNG DISEASE; CLINICAL CONDITIONS; COMPREHENSIVE COMPARISONS; DIFFERENT CLASS; LUNG INJURY; PATHOPHYSIOLOGY; SMALL ANIMAL; SMOKE INHALATION;

ANIMALS;

CIGARETTE SMOKE; EXPLOSIVE;

ACUTE DISEASE; ACUTE LUNG INJURY; ADULT RESPIRATORY DISTRESS SYNDROME; AIRWAY OBSTRUCTION; ANIMAL EXPERIMENT; ANIMAL MODEL; BRONCHIOLITIS OBLITERANS; CHEMICAL COMPOSITION; CHRONIC LUNG DISEASE; CLINICAL PROTOCOL; DISEASE SEVERITY; EPITHELIUM; EXPLOSION; HUMAN; LUNG BURN; LUNG DISEASE; MEDICAL RESEARCH; NONHUMAN; PNEUMONIA; PRIORITY JOURNAL; REVIEW; SCIENTIST; SEPSIS; TISSUE STRUCTURE; TRACHEA STENOSIS;

EID: 85034862717     PISSN: 0169409X     EISSN: 18728294     Source Type: Journal    
DOI: 10.1016/j.addr.2017.10.005     Document Type: Review

References (236)

1. de Carvalho, F.O., et al. Natural and synthetic products used for the treatment of smoke inhalation: a patent review. Expert Opin. Ther. Pat., 2017 (just-accepted).
2. Shirani, K.Z., Pruitt, B.A. Jr., Mason, A.D. Jr., The influence of inhalation injury and pneumonia on burn mortality. Ann. Surg., 205(1), 1987, 82.
3. Tanizaki, S., Assessing inhalation injury in the emergency room. Open Access Emerg. Med., 7, 2015, 31.
4. Association, A.B, Airway management and smoke inhalation injury. Advanced Burn Life Support Manual, 2004, Americal Burn Association, Chicago, 16–20.
5. Kraneveld, A., Nijkamp, F., Tachykinins and neuro-immune interactions in asthma. Int. Immunopharmacol. 1:9 (2001), 1629–1650.
6. Murakami, K., Traber, D.L., Pathophysiological basis of smoke inhalation injury. Physiology 18:3 (2003), 125–129.
7. Sakagami, M., In vivo, in vitro and ex vivo models to assess pulmonary absorption and disposition of inhaled therapeutics for systemic delivery. Adv. Drug Deliv. Rev. 58:9–10 (2006), 1030–1060.
8. Sporty, J.L., Horálková L., Ehrhardt, C., In vitro cell culture models for the assessment of pulmonary drug disposition. Expert Opin. Drug Metab. Toxicol. 4:4 (2008), 333–345.
9. Forbes, B., Human airway epithelial cell lines for in vitro drug transport and metabolism studies. Pharm. Sci. Technol. Today 3:1 (2000), 18–27.
10. Mendez, J.J., et al. Epithelial cell differentiation of human mesenchymal stromal cells in decellularized lung scaffolds. Tissue Eng. A 20:11 − 12 (2014), 1735–1746.
11. Hogan, B.L., et al. Repair and regeneration of the respiratory system: complexity, plasticity, and mechanisms of lung stem cell function. Cell Stem Cell 15:2 (2014), 123–138.
12. Hermanns, M.I., et al. Lung epithelial cell lines in coculture with human pulmonary microvascular endothelial cells: development of an alveolo-capillary barrier in vitro. Lab. Investig. 84:6 (2004), 736–752.
13. Benam, K.H., et al. Small airway-on-a-chip enables analysis of human lung inflammation and drug responses in vitro. Nat. Methods 13:2 (2016), 151–157.
14. Amann, A., et al. Development of an innovative 3D cell culture system to study tumour-stroma interactions in non-small cell lung cancer cells. PLoS One, 9(3), 2014, e92511.
15. Rutter, A.V., et al. Quantification by SIFT-MS of acetaldehyde released by lung cells in a 3D model. Analyst 138:1 (2013), 91–95.
16. Wirtz, H.R., Dobbs, L.G., Calcium mobilization and exocytosis after one mechanical stretch of lung epithelial cells. Science 250:4985 (1990), 1266–1270.
17. David, P., et al. Animal models of smoke inhalation induced injuries. Front. Biosci. (Landmark Ed.) 14 (2009), 4618–4630.
18. Kruger, A.W.H.a.C.L., Hayes’ Principles and Methods of Toxicology. Sixth Edition, 2014, CRC Press.
19. Bonfield, T.L., Irusen, Dr. Elvisegran Malcolm, (eds.) In Vivo Models of Lung Disease, Lung Diseases - Selected State of the Art Reviews, 2012.
20. Walker, P.F., et al. Diagnosis and management of inhalation injury: an updated review. Crit. Care, 19(1), 2015, 351.
21. Savolainen, H., Kirchner, N., Toxicological mechanisms of fire smoke. Internet J. Rescue Disaster Med., 1(1), 1997.
22. Prien, T., Traber, D.L., Toxic smoke compounds and inhalation injury—a review. Burns 14:6 (1988), 451–460.
23. Tiwari, A.J., Ashraf-Khorassani, M., Marr, L.C., C60 fullerenes from combustion of common fuels. Sci. Total Environ. 547 (2016), 254–260.
24. Sanderson, K., Carbon nanotubes: the new asbestos?. cited 2008; Available from http://www.nature.com/news/2008/080520/full/news.2008.845.html, 2008.
25. Magrez, A., et al. Cellular toxicity of carbon-based nanomaterials. Nano Lett. 6:6 (2006), 1121–1125.
26. Hubbard, G.B., et al. The morphology of smoke inhalation injury in sheep. J. Trauma Acute Care Surg. 31:11 (1991), 1477–1486.
27. Stephens, J., El-Shammaa, E., Carbon monoxide and cyanide poisoning in smoke inhalation victims. Trauma Reports, January 2015.
28. Atiyeh, B.S., Gunn, S.W.A., Hayek, S.N., Military and civilian burn injuries during armed conflicts. Ann. Burns Fire Disasters 20:4 (2007), 203–215.
29. Parrish, J.S., Bradshaw, D.A., Toxic inhalational injury: gas, vapor and vesicant exposure. Respir. Care Clin. N. Am. 10:1 (2004), 43–58.
30. Organisation, W.H, Household air pollution and health. Fact sheet No 292 2016 February 2016 23/06/2017; Available from: http://www.who.int/mediacentre/factsheets/fs292/en/.
31. Kocbach Bølling, A., et al. Health effects of residential wood smoke particles: the importance of combustion conditions and physicochemical particle properties. Part. Fibre Toxicol., 6(1), 2009, 29.
32. Dries, D.J., Endorf, F.W., Inhalation injury: epidemiology, pathology, treatment strategies. Scand. J. Trauma Resusc. Emerg. Med., 21, 2013.
33. Klein, K., et al. Feasibility study of a standardized novel animal model for cervical vertebral augmentation in sheep using a PTH derivate bioactive material. Vet. Sci. 1:2 (2014), 96–120.
34. Miller, A.C., Elamin, E.M., Suffredini, A.F., Inhaled anticoagulation regimens for the treatment of smoke inhalation-associated acute lung injury: a systematic review. Crit. Care Med. 42:2 (2014), 413–419.
35. Kimmel, E.C., Still, K.R., Acute lung injury, acute respiratory distress syndrome and inhalation injury: an overview. Drug Chem. Toxicol. 22:1 (1999), 91–128.
36. Mizutani, A., et al. Pulmonary changes in a mouse model of combined burn and smoke inhalation-induced injury. J. Appl. Physiol. (1985) 105:2 (2008), 678–684.
37. Burmeister, D.M. et al., A model of recovery from inhalation injury and cutaneous burn in ambulatory swine. 2017, Burns.
38. Belenkiy, S.M., et al. Acute respiratory distress syndrome in wartime military burns: application of the Berlin criteria. J. Trauma Acute Care Surg. 76:3 (2014), 821–827.
39. Zhu, F., et al. A rat model of smoke inhalation injury. Inhal. Toxicol. 24:6 (2012), 356–364.
40. Shimazu, T., et al. A dose-responsive model of smoke inhalation injury. Severity-related alteration in cardiopulmonary function. Ann. Surg. 206:1 (1987), 89–98.
41. Stec, A.A., Hull, T.R., Part II: harmful effects of fire effluents. Stec, A.A., Hull, T.R., (eds.) Fire Toxicity, 2010, Elsevier Science.
42. Schiff, L.J., Graham, J.A., Cytotoxic effect of vanadium and oil-fired fly ash on hamster tracheal epithelium. Environ. Res. 34:2 (1984), 390–402.
43. Phalen, R.F., Oldham, M.J., Tracheobronchial airway structure as revealed by casting techniques. Am. Rev. Respir. Dis. 128:2 Pt 2 (1983), S1–4.
44. Kling, M.A., A review of respiratory system anatomy, physiology, and disease in the mouse, rat, hamster, and gerbil. Vet. Clin. North Am. Exot. Anim. Pract. 14:2 (2011), 287–337.
45. Maynard, R.L., Comparative biology of the normal lung (treatise on pulmonary toxicology, volume 1). Occup. Environ. Med., 52(11), 1995, 783.
46. Nikula, K.J., et al. Lung tissue responses and sites of particle retention differ between rats and cynomolgus monkeys exposed chronically to diesel exhaust and coal dust. Toxicol. Sci. 37:1 (1997), 37–53.
47. Warheit, D.B., Hartsky, M.A., Species comparisons of proximal alveolar deposition patterns of inhaled particulates. Exp. Lung Res. 16:2 (1990), 83–99.
48. Ressmeyer, A.R., et al. Characterisation of guinea pig precision-cut lung slices: comparison with human tissues. Eur. Respir. J. 28:3 (2006), 603–611.
49. Wright, J.L., Cosio, M., Churg, A., Animal models of chronic obstructive pulmonary disease. Am. J. Phys. Lung Cell. Mol. Phys. 295:1 (2008), L1–L15.
50. Xie, E.F., et al. A rat model of smoke inhalation injury. Ann. Burns Fire Disasters, 11(2), 1998.
51. Matthew, E., Warden, G., Dedman, J., A murine model of smoke inhalation. Am. J. Phys. Lung Cell. Mol. Phys. 280:4 (2001), L716–L723.
52. Jacob, S., et al. Assessment of lung inflammation in a mouse model of smoke inhalation and burn injury: strain-specific differences. Toxicol. Mech. Methods 18:7 (2008), 551–559.
53. Jacob, S., et al. Mechanisms of toxic smoke inhalation and burn injury: role of neutral endopeptidase and vascular leakage in mice. Toxicol. Mech. Methods 19:3 (2009), 191–196.
54. Choi, W. II, et al. JNK activation is responsible for mucus overproduction in smoke inhalation injury. Respir. Res., 11(1), 2010, 172.
55. Moores, H.K., Janigan, D.T., Hajela, R.P., Lung injury after experimental smoke inhalation: particle-associated changes in alveolar macrophages. Toxicol. Pathol. 21:6 (1993), 521–527.
56. Hecht, S.S., Carcinogenicity studies of inhaled cigarette smoke in laboratory animals: old and new. Carcinogenesis 26:9 (2005), 1488–1492.
57. Sun, Y., et al. The effects of porcine pulmonary surfactant on smoke inhalation injury. J. Surg. Res. 198:1 (2015), 200–207.
58. Zhang, F., et al. Puerarin attenuates smoke inhalation injury by regulation of Th1/Th2 expression and inhibition of Th17 cells in rats. Int. Immunopharmacol. 28:1 (2015), 546–553.
59. Song, M., et al. Dynamic tracking human mesenchymal stem cells tropism following smoke inhalation injury in NOD/SCID mice. Stem Cells Int., 2016, 2016, 13.
60. Guénet, J.-L., Bonhomme, F., Chapter 1 - origin of the laboratory mouse and related subspecies A2 - Hedrich, Hans J. Bullock, G., (eds.) The Laboratory Mouse, 2004, Academic Press, London, 3–13.
61. Silver, L.M., Mouse Genetics: Concepts and Applications. 1995, Oxford University Press, New York.
62. Asmussen, S., et al. Human mesenchymal stem cells reduce the severity of acute lung injury in a sheep model of bacterial pneumonia. Thorax 69:9 (2014), 819–825.
63. Takahashi, A., et al. Changes in respiratory elastance after deep inspirations reflect surface film functionality in mice with acute lung injury. J. Appl. Physiol. (1985) 119:3 (2015), 258–265.
64. Gon, et al. Oleic acid induces lung injury in mice through activation of the ERK pathway. Mediat. Inflamm., 2012, 2012, 11.
65. Asti, C., et al. Lipopolysaccharide-induced lung injury in mice. I. Concomitant evaluation of inflammatory cells and haemorrhagic lung damage. Pulm. Pharmacol. Ther. 13:2 (2000), 61–69.
66. Cook, M.J., The Anatomy of Laboratory Mouse. 1965, Academic Press: M. R. C. Laboratory Animal Centre, Carshalton, Surrey, England.
67. Hyde, D.M., Hamid, Q., Irvin, C.G., Anatomy, pathology, and physiology of the tracheobronchial tree: emphasis on the distal airways. J. Allergy Clin. Immunol. 124:6 (2009), S72–S77.
68. Junqueira, L.C.U.a., Carneiro, José Histology. AccessMedicine, 11th ed., 2005, McGraw-Hill Companies, New York, c2005 (1920).
69. Irvin, C.G., Bates, J.H.T., Measuring the lung function in the mouse: the challenge of size. Respir. Res., 4(1), 2003, 4.
70. Abdi, S., et al. Inhalation injury to tracheal epithelium in an ovine model of cotton smoke exposure: early phase (30 minutes). Am. Rev. Respir. Dis. 142:6_pt_1 (1990), 1436–1439.
71. Alpard, S.K., et al. New clinically relevant sheep model of severe respiratory failure secondary to combined smoke inhalation/cutaneous flame burn injury. Crit. Care Med. 28:5 (2000), 1469–1476.
72. Murakami, K. et al., A novel animal model of sepsis after acute lung injury in sheep. Crit. Care Med. 30:9 (2002), 2083–2090.
73. Yahaya, B., Understanding cellular mechanisms underlying airway epithelial repair: selecting the most appropriate animal models. Sci. World J., 2012, 2012, 961684.
74. Po, J.Y., FitzGerald, J.M., Carlsten, C., Respiratory disease associated with solid biomass fuel exposure in rural women and children: systematic review and meta-analysis. Thorax 66:3 (2011), 232–239.
75. Kurmi, O.P., et al. COPD and chronic bronchitis risk of indoor air pollution from solid fuel: a systematic review and meta-analysis. Thorax 65:3 (2010), 221–228.
76. Hu, G., et al. Risk of COPD from exposure to biomass smoke: a metaanalysis. Chest 138:1 (2010), 20–31.
77. Peters, L.L., et al. The mouse as a model for human biology: a resource guide for complex trait analysis. Nat. Rev. Genet. 8:1 (2007), 58–69.
78. Flint, J., Eskin, E., Genome-wide association studies in mice. Nat. Rev. Genet. 13:11 (2012), 807–817.
79. Meeusen, E.N., et al. Sheep as a model species for the study and treatment of human asthma and other respiratory diseases. Drug Discov. Today Dis. Model. 6:4 (2009), 101–106.
80. Matute-Bello, G., Frevert, C.W., Martin, T.R., Animal models of acute lung injury. Am. J. Phys. Lung Cell. Mol. Phys. 295:3 (2008), L379–L399.
81. Lim, R., et al. Measuring respiratory function in mice using unrestrained whole-body plethysmography. J. Vis. Exp., 90, 2014, 51755.
82. Pouwels, S.D., et al. Genetic variation associates with susceptibility for cigarette smoke-induced neutrophilia in mice. Am. J. Phys. Lung Cell. Mol. Phys. 308:7 (2015), L693–L709.
83. Lee, H.M., et al. A rat model of smoke inhalation injury: influence of combustion smoke on gene expression in the brain. Toxicol. Appl. Pharmacol. 208:3 (2005), 255–265.
84. Chen, X., et al. Protective effects of hydrogen-rich saline on rats with smoke inhalation injury. Oxidative Med. Cell. Longev., 2015, 2015, 8.
85. Dubick, M.A., et al. Indices of antioxidant status in rats subjected to wood smoke inhalation and/or thermal injury. Toxicology 176:1 (2002), 145–157.
86. Belli, S., et al. Protective role of simvastatin on lung damage caused by burn and cotton smoke inhalation in rats. J. Surg. Res. 167:2 (2011), e283–e290.
87. Wallingford, J.B., Liu, K.J., Zheng, Y., Xenopus. Curr. Biol. 20:6 (2010), R263–R264.
88. Harland, R.M., Grainger, R.M., Xenopus research: metamorphosed by genetics and genomics. Trends Genet. 27:12 (2011), 507–515.
89. Hoymann, H.G., Lung function measurements in rodents in safety pharmacology studies. Front. Pharmacol., 3, 2012, 156.
90. Nakakuki, S., The bronchial tree and blood vessels of the rat lung. Anat. Anz. 154:4 (1983), 305–312.
91. Hofmann, W., Koblinger, L., Martonen, T.B., Structural differences between human and rat lungs: implications for Monte Carlo modeling of aerosol deposition. Health Phys. 57:Suppl. 1 (1989), 41–46 (discussion 46-7).
92. Chen, X., et al. Protective effects of hydrogen-rich saline on rats with smoke inhalation injury. Oxidative Med. Cell. Longev., 2015, 2015, 106836.
93. Cetin, C., et al. Effects of rolling inhibition on smoke inhalation injury. Burns 29:4 (2003), 307–314.
94. Tuggle, K.L., et al. Characterization of defects in ion transport and tissue development in cystic fibrosis transmembrane conductance regulator (CFTR)-knockout rats. PLoS One, 9(3), 2014, e91253.
95. Iannaccone, P.M., Jacob, H.J., Rats!. Dis. Model. Mech. 2:5–6 (2009), 206–210.
96. Gonzalez-Garcia, M., et al. Prevalence, risk factors and underdiagnosis of asthma and wheezing in adults 40 years and older: a population-based study. J. Asthma 52:8 (2015), 823–830.
97. Kucharewicz, I., Bodzenta-Lukaszyk, A., Buczko, W., Experimental asthma in rats. Pharmacol. Rep. 60:6 (2008), 783–788.
98. Homberg, J.R., Wohr, M., Alenina, N., Comeback of the rat in biomedical research. ACS Chem. Neurosci. 8:5 (2017), 900–903.
99. Groneberg, D.A., Chung, K.F., Models of chronic obstructive pulmonary disease. Respir. Res., 5(1), 2004, 18.
100. Shubik, P., et al. Factors determining the neoplastic response induced by carcinogens. Brennan, M.J., Simpson, W.L., (eds.) Biological Interactions in Normal and Neoplastic Growth, 1962, Little, Brown and Co., Boston, 285–297.
101. Montesano, R., Saffiotti, U., Shubik, P., The role of topical and systemic factors in experimental respiratory carcinogenesis. Inhalation Carcinogenesis, 1970, US Atomic Energy Comm. Div. Techn. Inform. Extension, Oak Ridge, Tennessee, 353–371.
102. Griffey, S.M., Kraegel, S.A., Madewell, B.R., Rapid detection of K-ras gene mutations in canine lung cancer using single-strand conformational polymorphism analysis. Carcinogenesis 19:6 (1998), 959–963.
103. Warner, B.M., Safronetz, D., Kobinger, G.P., Syrian hamsters as a small animal model for emerging infectious diseases: advances in immunologic methods. Rezza, G., Ippolito, G., (eds.) Emerging and Re-emerging Viral Infections: Advances in Microbiology, Infectious Diseases and Public Health, Vol. 6, 2017, Springer International Publishing, Cham, 87–101.
104. Bhathena, J., et al. Diet-induced metabolic hamster model of nonalcoholic fatty liver disease. Diabetes Metab. Syndr. Obes. 4 (2011), 195–203.
105. Dillard, A., Matthan, N.R., Lichtenstein, A.H., Use of hamster as a model to study diet-induced atherosclerosis. Nutr. Metab. (Lond.), 7, 2010, 89.
106. Jove, M., et al. Lipidomic and metabolomic analyses reveal potential plasma biomarkers of early atheromatous plaque formation in hamsters. Cardiovasc. Res. 97:4 (2013), 642–652.
107. Staffend, N.A., Meisel, R.L., Aggressive experience increases dendritic spine density within the nucleus accumbens core in female Syrian hamsters. Neuroscience 227 (2012), 163–169.
108. Vijayalingam, S., et al. Evaluation of apoptogenic adenovirus type 5 oncolytic vectors in a Syrian hamster head and neck cancer model. Cancer Gene Ther. 21:6 (2014), 228–237.
109. Kuehne, S.A., et al. Importance of toxin A, toxin B, and CDT in virulence of an epidemic Clostridium difficile strain. J Infect Dis 209:1 (2014), 83–86.
110. Safronetz, D., et al. Adenovirus vectors expressing hantavirus proteins protect hamsters against lethal challenge with andes virus. J. Virol. 83:14 (2009), 7285–7295.
111. Dondji, B., et al. Role for nitric oxide in hookworm-associated immune suppression. Infect. Immun. 76:6 (2008), 2560–2567.
112. Safronetz, D., et al. The Syrian hamster model of hantavirus pulmonary syndrome. Antivir. Res. 95:3 (2012), 282–292.
113. Kennedy, A.R., et al. Morphometric and histological analysis of the lungs of Syrian golden hamsters. J. Anat. 125:Pt 3 (1978), 527–553.
114. McPherson, C.W., Van Hoosier, G.L., Laboratory Hamsters. 1987, Academic Press, Orlando.
115. Reznik-Schüller, H., Ciliary alterations in hamster respiratory tract epithelium after exposure to carcinogens and cigarette smoke. Cancer Lett. 1 (1975), 7–13.
116. Becci, P.J., McDowell, E.M., Trump, B.F., The respiratory epithelium. II. Hamster trachea, bronchus, and bronchioles. J. Natl. Cancer Inst. 61:2 (1978), 551–561.
117. Bernfeld, P., et al. Cigarette smoke inhalation studies in inbred Syrian golden hamsters. J. Natl. Cancer Inst. 63:3 (1979), 675–689.
118. Dontenwill, W., et al. Investigations on the effects of chronic cigarette-smoke inhalation in Syrian golden hamsters. J. Natl. Cancer Inst. 51:6 (1973), 1781–1832.
119. Lehr, H.-A., et al. Cigarette smoke elicits leukocyte adhesion to endothelium in hamsters: inhibition by CuZn-SOD. Free Radic. Biol. Med. 14:6 (1993), 573–581.
120. Reznik-Schuller, H.M., Acute effects of cigarette smoke inhalation on the Syrian hamster lungs. J. Environ. Pathol. Toxicol. 4:1 (1980), 285–291.
121. Tabassian, A.R., et al. Evidence for cigarette smoke-induced calcitonin secretion from lungs of man and hamster. Life Sci. 42:23 (1988), 2323–2329.
122. Brightwell, J., et al. Tumours of the respiratory tract in rats and hamsters following chronic inhalation of engine exhaust emissions. J. Appl. Toxicol. 9:1 (1989), 23–31.
123. Brain, J.D., et al. Pulmonary toxicity in hamsters of smoke particles from Kuwaiti oil fires. Environ. Health Perspect. 106:3 (1998), 141–146.
124. Harada, T., Meade, P.D., Basrur, P.K., Effect of vitamin A on pulmonary macrophage mobilization in hamsters exposed to cigarette smoke. J. Toxicol. Pathol. 10:4 (1997), 193–198.
125. Wehner, A.P., et al. Acute and subchronic inhalation exposures of hamsters to nickel-enriched fly ash. Environ. Res. 19:2 (1979), 355–370.
126. Safronetz, D., et al. In vitro and in vivo activity of ribavirin against Andes virus infection. PLoS One, 6(8), 2011, e23560.
127. Sørensen, D.B., et al. An ethological approach to housing requirements of golden hamsters, Mongolian gerbils and fat sand rats in the laboratory—a review. Appl. Anim. Behav. Sci. 94:3 (2005), 181–195.
128. Kim, J., Kim, Y., Animal models in carotenoids research and lung cancer prevention. Transl. Oncol. 4:5 (2011), 271–281.
129. Adissu, H.A., Schuller, H.M., Antagonistic growth regulation of cell lines derived from human lung adenocarcinomas of Clara cell and aveolar type II cell lineage: implications for chemoprevention. Int. J. Oncol. 24:6 (2004), 1467–1472.
130. Schuller, H.M., et al. Pathobiology of lung tumors induced in hamsters by 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone and the modulating effect of hyperoxia. Cancer Res. 50:6 (1990), 1960–1965.
131. Cambau, E., Drancourt, M., Steps towards the discovery of Mycobacterium tuberculosis by Robert Koch, 1882. Clin. Microbiol. Infect. 20:3 (2014), 196–201.
132. Padilla-Carlin, D.J., McMurray, D.N., Hickey, A.J., The guinea pig as a model of infectious diseases. Comp. Med. 58:4 (2008), 324–340.
133. Gray, T., Garber, S., A brief history of animals in space. Available from: National Aeronautics and Space Administration http://history.nasa.gov/animals.html, 1998.
134. Torres-Duque, C.A., Garcia-Rodriguez, M.C., Gonzalez-Garcia, M., Is chronic obstructive pulmonary disease caused by wood smoke a different phenotype or a different entity?. Arch. Bronconeumol. 52:8 (2016), 425–431.
135. Ordway, D.J., et al. Evaluation of standard chemotherapy in the guinea pig model of tuberculosis. Antimicrob. Agents Chemother. 54:5 (2010), 1820–1833.
136. Yarto-Jaramillo, E., Respiratory system anatomy, physiology, and disease: guinea pigs and chinchillas. Vet. Clin. North Am. Exot. Anim. Pract. 14:2 (2011), 339–355 (vi).
137. Schreider, J.P., Hutchens, J.O., Morphology of the guinea pig respiratory tract. Anat. Rec. 196:3 (1980), 313–321.
138. Brewer, N.R., Cruise, L.J., The respiratory system of the guinea pig: emphasis on species differences. J. Am. Assoc. Lab. Anim. Sci. 36:1 (1997), 100–108.
139. Hsu, T.H., Lai, Y.L., Kou, Y.R., Smoke-induced airway hyperresponsiveness to inhaled wood smoke in guinea pigs: tachykininergic and cholinergic mechanisms. Life Sci. 63:17 (1998), 1513–1524.
140. Hsu, T.H., Kou, Y.R., Airway hyperresponsiveness to bronchoconstrictor challenge after wood smoke exposure in guinea pigs. Life Sci. 68:26 (2001), 2945–2956.
141. Hsu, T.H., Lai, Y.L., Kou, Y.R., Wood smoke-induced airway hyperreactivity in guinea pigs: time course, and role of leukotrienes and hydroxyl radical. Life Sci. 66:11 (2000), 971–980.
142. Kou, Y.R., Lai, C.J., Reflex changes in breathing pattern evoked by inhalation of wood smoke in rats. J. Appl. Physiol. (1985) 76:6 (1994), 2333–2341.
143. 2 challenges. Toxicol. Appl. Pharmacol. 75:1 (1984), 69–80.
144. Burns, A.R., et al. Respiratory epithelial permeability after cigarette smoke exposure in guinea pigs. J. Appl. Physiol. (1985) 66:5 (1989), 2109–2116.
145. Fryer, A.D., Jacoby, D.B., Parainfluenza virus infection damages inhibitory M2 muscarinic receptors on pulmonary parasympathetic nerves in the guinea-pig. Br. J. Pharmacol. 102:1 (1991), 267–271.
146. Kibler, H.H., Brody, S., Worstell, D., Surface area and metabolism of growing guinea pigs. J. Nutr. 33:3 (1947), 331–338.
147. Wright, J.L., Churg, A., Cigarette smoke causes physiologic and morphologic changes of emphysema in the guinea pig. Am. Rev. Respir. Dis., 142, 1990.
148. Canning, B.J., Chou, Y., Using guinea pigs in studies relevant to asthma and COPD. Pulm. Pharmacol. Ther. 21:5 (2008), 702–720.
149. McMurray, D.N., Guinea pig model of tuberculosis. Tuberculosis, 1994, American Society of Microbiology.
150. McMurray, D.N., Disease model: pulmonary tuberculosis. Trends Mol. Med. 7:3 (2001), 135–137.
151. Shomer, N.H., Holcombe, H., Harkness, J.E., Chapter 6 - biology and diseases of guinea pigs A2 - Fox, James G. Anderson, L.C., et al. (eds.) Laboratory Animal Medicine, Third Edition, 2015, Academic Press, Boston, 247–283.
152. Nambiar, M.P., et al. A simple method for accurate endotracheal placement of an intubation tube in Guinea pigs to assess lung injury following chemical exposure. Toxicol. Mech. Methods 17:7 (2007), 385–392.
153. Blouin, A., Cormier, Y., Endotracheal intubation in guinea pigs by direct laryngoscopy. Lab. Anim. Sci. 37:2 (1987), 244–245.
154. Goldklang, M., Marks, S., D'Armiento, J., Second hand smoke and COPD: lessons from animal studies. Front. Physiol., 2013, 4(30).
155. Kozma, C., et al. Anatomy, physiology, and biochemistry of the rabbit. The Biology of the Laboratory Rabbit, 1974, 49–72.
156. Parent, R.A., Comparative Biology of the Normal Lung. 2015, Academic Press.
157. Liu, Q., et al. Functional residual capacity in beagle dogs with and without acute respiratory distress syndrome. J. Thorac. Dis. 7:8 (2015), 1459–1466.
158. Patra, A.L., Comparative anatomy of mammalian respiratory tracts: the nasopharyngeal region and the tracheobronchial region. J. Toxicol. Environ. Health Part A Curr. Issues 17:2–3 (1986), 163–174.
159. Pittet, J.-F., et al. Resistance of the alveolar epithelium to injury from septic shock in sheep. Am. J. Respir. Crit. Care Med. 151:4 (1995), 1093–1100.
160. Hare, W., The broncho-pulmonary segments in the sheep. J. Anat., 89(Pt 3), 1955, 387.
161. Asgharian, B., et al. Development of a rhesus monkey lung geometry model and application to particle deposition in comparison to humans. Inhal. Toxicol. 24:13 (2012), 869–899.
162. Enkhbaatar, P., et al. Aerosolized tissue plasminogen inhibitor improves pulmonary function in sheep with burn and smoke inhalation. Shock, 22, 2004.
163. Schmidt-Nielsen, K., Animal Physiology: Adaptation and Environment. 1997, Cambridge University Press.
164. Plopper, C.G., et al. Cytodifferentiation of the nonciliated bronchiolar epithelial (Clara) cell during rabbit lung maturation: an ultrastructural and morphometric study. Dev. Dyn. 167:3 (1983), 329–357.
165. Clermont, Y., Lalli, M., Bencsath-Makkai, Z., Light-microscopy histology atlas. Available from: http://audilab.bmed.mcgill.ca/HA/html/HAintro_E.html, 2009.
166. Mariassy, A.T., Plopper, C.G., Tracheobronchial epithelium of the sheep: I. Quantitative light-microscopic study of epithelial cell abundance, and distribution. Anat. Rec. 205:3 (1983), 263–275.
167. Plopper, C.G., Hyde, D.M., The non-human primate as a model for studying COPD and asthma. Pulm. Pharmacol. Ther. 21:5 (2008), 755–766.
168. Laffon, M., et al. Interleukin-8 mediates injury from smoke inhalation to both the lung endothelial and the alveolar epithelial barriers in rabbits. Am. J. Respir. Crit. Care Med. 160:5 (1999), 1443–1449.
169. Sakano, T., et al. A rabbit model of inhalation injury. J. Trauma Acute Care Surg. 34:3 (1993), 411–416.
170. Davies, L.K., Poulton, T.J., Modell, J.H., Continuous positive airway pressure is beneficial in treatment of smoke inhalation. Crit. Care Med. 11:9 (1983), 726–729.
171. Nie, F., et al. Early high volume lung lavage for acute severe smoke inhalation injury in dogs. Mol. Med. Rep. 9:3 (2014), 863–871.
172. Hammond, E., et al. Effects of cigarette smoking on dogs. I. Design of experiment, mortality, and findings in lung parenchyma. Arch. Environ. Health 21:6 (1970), 740–753.
173. Brizio-Molteni, L., et al. Effect of wood combustion smoke inhalation on angiotensin-1-converting enzyme in the dog. Ann. Clin. Lab. Sci. 14:5 (1984), 381–389.
174. Shimoda, K., et al. Effect of poly(ADP ribose) synthetase inhibition on burn and smoke inhalation injury in sheep. Am. J. Phys. Lung Cell. Mol. Phys. 285:1 (2003), L240–L249.
175. Palmieri, T.L., et al. Continuous nebulized albuterol attenuates acute lung injury in an ovine model of combined burn and smoke inhalation. Crit. Care Med. 34:6 (2006), 1719–1724.
176. Enkhbaatar, P., et al. Aerosolized tissue plasminogen inhibitor improves pulmonary function in sheep with burn and smoke inhalation. Shock 22:1 (2004), 70–75.
177. Murakami, K., et al. Heparin nebulization attenuates acute lung injury in sepsis following smoke inhalation in sheep. Shock 18:3 (2002), 236–241.
178. Batchinsky, A.I., et al. Comparison of airway pressure release ventilation to conventional mechanical ventilation in the early management of smoke inhalation injury in swine. Crit. Care Med. 39:10 (2011), 2314–2321.
179. Linden, K., et al. Evaluation of the Cytosorb™ hemoadsorptive column in a PIG model of severe smoke and burn injury. Shock 44:5 (2015), 487–495.
180. Belenkiy, S., et al. Noninvasive carbon dioxide monitoring in a porcine model of acute lung injury due to smoke inhalation and burns. Shock 39:6 (2013), 495–500.
181. Jeng, M.J., et al. Effects of perfluorochemical evaporative properties on oxygenation during partial liquid ventilation. Pediatr. Int. 48:6 (2006), 608–615.
182. Raymond, T.L., Delucia, A.J., Bryant, L.R., Failure of chronic cigarette smoke exposure to alter plasma lipoproteins of stumptailed macaques (Macaca arctoides). Atherosclerosis 41:1 (1982), 27–33.
183. Hubbard, G.B., et al. The morphology of smoke inhalation injury in sheep. J. Trauma Acute Care Surg. 31:11 (1991), 1477–1486.
184. Bidani, A., et al. Dose dependence and time course of smoke inhalation injury in a rabbit model. Lung 177:2 (1999), 111–122.
185. Loke, J., et al. Rabbit lung after acute smoke inhalation: cellular responses and scanning electron microscopy. Arch. Surg. 119:8 (1984), 956–959.
186. Mapara, M., Thomas, B.S., Bhat, K.M., Rabbit as an animal model for experimental research. Dent. Res. J. 9:1 (2012), 111–118.
187. Cryan, S.A., Sivadas, N., Garcia-Contreras, L., In vivo animal models for drug delivery across the lung mucosal barrier. Adv. Drug Deliv. Rev. 59:11 (2007), 1133–1151.
188. Calasans-Maia, M.D., et al. The rabbit as an animal model for experimental surgery. Acta Cir. Bras. 24:4 (2009), 325–328.
189. Yanni, A.E., The laboratory rabbit: an animal model of atherosclerosis research. Lab. Anim. 38:3 (2004), 246–256.
190. Fan, J., Watanabe, T., Transgenic rabbits as therapeutic protein bioreactors and human disease models. Pharmacol. Ther. 99:3 (2003), 261–282.
191. Chen, Q., et al. High-resolution computed tomography of the mammalian lung. Am. J. Vet. Res. 53:7 (1992), 1218–1224.
192. Kozma, C., et al. Anatomy, physiology and biochemistry of the rabbit. The Biology of the Laboratory Rabbit, 1974, 49–72.
193. Kamaruzaman, N.A., et al. The rabbit as a model for studying lung disease and stem cell therapy. Biomed. Res. Int., 2013, 2013, 691830.
194. Ramchandani, R., et al. Airway branching morphology of mature and immature rabbit lungs. J. Appl. Physiol. 90:4 (2001), 1584–1592.
195. McLaughlin, R.F. Jr., Tyler, W.S., Canada, R.O., Subgross pulmonary anatomy of the rabbit, rat, and guinea pig, with additional notes on the human lung 1, 2, 3. Am. Rev. Respir. Dis. 94:3 (1966), 380–387.
196. Hilding, D.A., Hilding, A.C., Electron microscopic observations of nasal epithelium after experimental alteration of airflow. Ann. Otol. Rhinol. Laryngol. 79:3 (1970), 451–460.
197. Dion, G.R., et al. Development of an in vivo model of laryngeal burn injury. Laryngoscope 127:1 (2017), 186–190.
198. Thorning, D.R., et al. Pulmonary responses to smoke inhalation: morphologic changes in rabbits exposed to pine wood smoke. Hum. Pathol. 13:4 (1982), 355–364.
199. Fick, R.B. Jr., et al. Alterations in the antibacterial properties of rabbit pulmonary macrophages exposed to wood smoke 1, 2. Am. Rev. Respir. Dis. 129:1 (1984), 76–81.
200. Iskander, N.M., et al. Evaluation of the effect of cigarette smoking on the olfactory neuroepithelium of New Zealand white rabbit, using scanning electron microscope. Eur. Arch. Otorhinolaryngol. 274:6 (2017), 2461–2468.
201. Bidani, A., Wang, C., Heming, T., Early effects of smoke inhalation on alveolar macrophage functions. Burns 22:2 (1996), 101–106.
202. Keir, S., Page, C., The rabbit as a model to study asthma and other lung diseases. Pulm. Pharmacol. Ther. 21:5 (2008), 721–730.
203. Keir, S.D., et al. Airway responsiveness in an allergic rabbit model. J. Pharmacol. Toxicol. Methods 64:2 (2011), 187–195.
204. Murdock, H.R. Jr., Anesthesia in the rabbit. Fed. Proc. 28:4 (1969), 1510–1516.
205. Guillaumin, J., Hopper, K., Successful outcome in a dog with neurological and respiratory signs following smoke inhalation. J. Vet. Emerg. Crit. Care 23:3 (2013), 328–334.
206. Mariani, C.L., Full recovery following delayed neurologic signs after smoke inhalation in a dog. J. Vet. Emerg. Crit. Care 13:4 (2003), 235–239.
207. Mukaratirwa, S., et al. Spontaneous and dosing route-related lung lesions in beagle dogs from oral gavage and inhalation toxicity studies: differentiation from compound-induced lesions. Toxicol. Pathol. 44:7 (2016), 962–973.
208. Coggins, C.R., A review of chronic inhalation studies with mainstream cigarette smoke, in hamsters, dogs, and nonhuman primates. Toxicol. Pathol. 29:5 (2001), 550–557.
209. Zwicker, G., et al. Clinical and pathological effects of cigarette smoke exposure in beagle dogs. Arch. Pathol. Lab. Med. 102:12 (1978), 623–628.
210. Park, S.S., et al. An animal model of cigarette smoking in beagle dogs: correlative evaluation of effects on pulmonary function, defense, and morphology 1, 2. Am. Rev. Respir. Dis. 115:6 (1977), 971–979.
211. Auerbach, O., et al. Histologic changes in bronchial tubes of cigarette-smoking dogs. Cancer 20:12 (1967), 2055–2066.
212. Auerbach, O., et al. Emphysema produced in dogs by cigarette smoking. JAMA 199:4 (1967), 241–246.
213. Welsh, M., Cigarette smoke inhibition of ion transport in canine tracheal epithelium. J. Clin. Investig., 71(6), 1983, 1614.
214. Forbes, R.B., Murray, D.J., Albanese, M.A., Evaluation of an animal model for teaching fibreoptic tracheal intubation. Can. J. Anaesth., 36(2), 1989, 141.
215. Kuehl, P.J., et al. Formulation development and in vivo evaluation of a new dry powder formulation of albuterol sulphate in beagle dogs. Pharm. Res. 27:5 (2010), 894–904.
216. Surendrakumar, K., et al. Sustained release of insulin from sodium hyaluronate based dry powder formulations after pulmonary delivery to beagle dogs. J. Control. Release 91:3 (2003), 385–394.
217. Skorohod, N., Yeates, D.B., Superoxide dismutase failed to attenuate allergen-induced nasal congestion in ragweed-sensitized dogs. J. Appl. Physiol. 98:4 (2005), 1478–1486.
218. Adjei, A., et al. Bioavailability of leuprolide following intratracheal administration to beagle dogs. Int. J. Pharm. 61:1 (1990), 135–144.
219. Paoloni, M., Khanna, C., Translation of new cancer treatments from pet dogs to humans. Nat. Rev. Cancer 8:2 (2008), 147–156.
220. Schiffman, J.D., Breen, M., Comparative oncology: what dogs and other species can teach us about humans with cancer. Philos. Trans. R. Soc. B, 370(1673), 2015, 20140231.
221. Lindblad-Toh, K., et al. Genome sequence, comparative analysis and haplotype structure of the domestic dog. Nature 438:7069 (2005), 803–819.
222. Schoenebeck, J.J., Ostrander, E.A., Insights into morphology and disease from the dog genome project. Annu. Rev. Cell Dev. Biol. 30 (2014), 535–560.
223. Koenig, E.M., et al. The beagle dog MicroRNA tissue atlas: identifying translatable biomarkers of organ toxicity. BMC Genomics, 17(1), 2016, 649.
224. Kol, A., et al. Companion animals: translational scientist's new best friends. Sci. Transl. Med., 7(308), 2015, 308ps21.
225. Meeusen, E.N., et al. Sheep as a model species for the study and treatment of human asthma and other respiratory diseases. Drug Discov. Today Dis. Model. 6:4 (2010), 101–106.
226. Nowell, J.A., Tyler, W.S., Scanning electron microscopy of the surface morphology of mammalian lungs. Am. Rev. Respir. Dis. 103:3 (1971), 313–328.
227. Gil, J., Models of lung disease: microscopy and structural methods. Thorax, 46(8), 1991, 611.
228. Garcia-Contreras, L., In vivo animal models for controlled-release pulmonary drug delivery. Smyth, D.C.H., Hickey, J.A., (eds.) Controlled Pulmonary Drug Delivery, 2011, Springer New York, New York, NY, 443–474.
229. Dassow, C., et al. Comparison of airway responses in sheep of different age in precision-cut lung slices (PCLS). Am. J. Respir. Crit. Care Med., 181, 2010, A5031.
230. Maybauer, M.O., et al. Recombinant human activated protein C improves pulmonary function in ovine acute lung injury resulting from smoke inhalation and sepsis. Crit. Care Med. 34:9 (2006), 2432–2438.
231. Soejima, K., et al. Role of nitric oxide in vascular permeability after combined burns and smoke inhalation injury. Am. J. Respir. Crit. Care Med. 163:3 Pt 1 (2001), 745–752.
232. Steinberg, J.M., et al. Wood smoke inhalation causes alveolar instability in a dose-dependent fashion. Respir. Care 50:8 (2005), 1062–1070.
233. Ando, K., Yanagita, T., Cigarette smoking in rhesus monkeys. Psychopharmacology 72:2 (1981), 117–127.
234. Ryan, G.M., et al. A Comparison of the Pharmacokinetics and Pulmonary Lymphatic Exposure of a Generation 4 PEGylated Dendrimer Following Intravenous and Aerosol Administration to Rats and Sheep. Pharm. Res. 33:2 (2016), 510–525.
235. McDonald, C.I., et al. The impact of acute lung injury, ECMO and transfusion on oxidative stress and plasma selenium levels in an ovine model. J. Trace Elem. Med. Biol. 30 (2015), 4–10.
236. Schreier, H., et al. Pharmacokinetics of detirelix following intratracheal instillation and aerosol inhalation in the unanesthetized awake sheep. Pharm. Res. 11:7 (1994), 1056–1059.