Cigarette smoke induced genotoxicity and respiratory tract pathology: evidence to support reduced exposure time and animal numbers in tobacco product testing

References

• Aoshiba K, Nagai A. (2003). Oxidative stress, cell death, and other damage to alveolar epithelial cells induced by cigarette smoke. Tob Induc Dis 1:219–26
   PubMedGoogle Scholar
• Ayres PH, Hayes JR, Higuchi MA, et al. (2001). Subchronic inhalation by rats of mainstream smoke from a cigarette that primarily heats tobacco compared to a cigarette that burns tobacco. Inhal Toxicol 13:149–86
   PubMed Web of Science ®Google Scholar
• Baker RR, Massey ED, Smith G. (2004). An overview of the effects of tobacco ingredients on smoke chemistry and toxicity. Food Chem Toxicol 42:S53–83
   PubMed Web of Science ®Google Scholar
• Baxter A, Thain S, Banerjee A, et al. (2015). Targeted omics analyses, and metabolic enzyme activity assays demonstrate maintenance of key muco-ciliary characteristics in long-term cultures of reconstituted human airway epithelia. Toxicol In Vitro 29:864–75
   PubMed Web of Science ®Google Scholar
• Boletín Oficial Del Estado. (2013). Por el que se establecen las normas básicas aplicables para la protección de los animales utilizados en experimentación y otros fines científicos, incluyendo la docencia. Available from: https://www.boe.es/diario_boe/txt.php?id=BOE-A-2013-1337. [Last accessed: 27 Apr 2016]
   Google Scholar
• Bright J, Aylott M, Bate S, et al. (2011). Recommendations on the statistical analysis of the Comet assay. Pharm Stat 10:485–93
   PubMed Web of Science ®Google Scholar
• Dalrymple A, Ordonez P, Thorne D, et al. (2015). An improved method for the isolation of rat alveolar type II lung cells: use in the Comet assay to determine DNA damage induced by cigarette smoke. Regul Toxicol Pharmacol 72:141–9
   PubMed Web of Science ®Google Scholar
• DeMarini DM. (2004). Genotoxicity of tobacco smoke and tobacco smoke condensate: a review. Mutat Res 567:447–74
   PubMed Web of Science ®Google Scholar
• Dertinger SD, Camphausen K, MacGregor JT, et al. (2004). Three-color labeling method for flow cytometric measurement of cytogenetic damage in rodent and human blood. Environ Mol Mutagen 44:427–35
   PubMed Web of Science ®Google Scholar
• Dertinger SD, Phonethepswath S, Avlasevich SL, et al. (2012). Efficient monitoring of in vivo pig-a gene mutation and chromosomal damage: summary of 7 published studies and results from 11 new reference compounds. Toxicol Sci 130:328–48
   PubMed Web of Science ®Google Scholar
• Dvorak A, Tilley AE, Shaykhiev R, et al. (2011). Do airway epithelium air–liquid cultures represent the in vivo airway epithelium transcriptome? Am J Respir Cell Mol Biol 44:465–73
   PubMed Web of Science ®Google Scholar
• European Union. (2010). Directive 2010/63/EU Of The European Parliament and of the Council on the protection of animals used for scientific purposes. Available from: http://ec.europa.eu/environment/chemicals/lab_animals/legislation_en.htm. [Last accessed: 27 Apr 2016]
   Google Scholar
• Fujimoto H, Tsuji H, Okubo C, et al. (2015). Biological responses in rats exposed to mainstream smoke from a heated cigarette compared to a conventional reference cigarette. Inhal Toxicol 27:224–36
   PubMed Web of Science ®Google Scholar
• Gaworski CL, Schramke H, Diekmann J, et al. (2009). Effect of filtration by activated charcoal on the toxicological activity of cigarette mainstream smoke from experimental cigarettes. Inhal Toxicol 21:688–704
   PubMed Web of Science ®Google Scholar
• Gollapudi BB, Lynch AM, Heflich RH, et al. (2015). The in vivo Pig-a assay: a report of the International Workshop On Genotoxicity Testing (IWGT) Workgroup. Mutat Res Genet Toxicol Environ Mutagen 783:23–35
   PubMed Web of Science ®Google Scholar
• Gruver AL, Sempowski GD. (2008). Cytokines, leptin, and stress-induced thymic atrophy. J Leukoc Biol 84:915–23
   PubMed Web of Science ®Google Scholar
• ICH (International Conference on Harmonization) (2011). Guidance on genotoxicity testing and data interpretation for pharmaceuticals intended for human use S2(R1). International Conference On Harmonization
   Google Scholar
• Institute of Medicine (2001). Clearing the smoke: the science base for tobacco harm reduction. Washington, DC: National Academic Press
   Google Scholar
• International Organization for Standardization (1999). ISO 3402:1999 – tobacco and tobacco products – atmosphere for conditioning and testing. Available from: http://www.iso.org/iso/catalogue_detail.htm?csnumber=28324. [Last accessed: 27 Apr 2016]
   Google Scholar
• International Organization for Standardization (2000a). ISO 3308:2000 – routine analytical cigarette-smoking machine: definitions and standard conditions. Available from: http://www.iso.org/iso/iso_catalogue/catalogue_ics/catalogue_detail_ics.htm?csnumber=28325. [Last accessed: 27 Apr 2016]
   Google Scholar
• International Organization for Standardization (2000b). ISO 4387:2000 – cigarettes: determination of total and nicotine-free dry particulate matter using a routine analytical smoking machine. Available from: http://www.iso.org/iso/iso_catalogue/catalogue_tc/catalogue_detail.htm?csnumber=28323. [Last accessed: 27 Apr 2016]
   Google Scholar
• Kamp DW, Greenberger MJ, Sbalchierro JS, et al. (1998). Cigarette smoke augments asbestos-induced alveolar epithelial cell injury: role of free radicals. Free Radic Biol Med 25:728–39
   PubMed Web of Science ®Google Scholar
• Kogel U, Schlage WK, Martin F, et al. (2014). A 28-day rat inhalation study with an integrated molecular toxicology endpoint demonstrates reduced exposure effects for a prototypic modified risk tobacco product compared with conventional cigarettes. Food Chem Toxicol 68:204–17
   PubMed Web of Science ®Google Scholar
• Kuehn D, Majeed S, Guedj E, et al. (2015). Impact assessment of repeated exposure of organotypic 3D bronchial and nasal tissue culture models to whole cigarette smoke. J Vis Exp 12:96
   Google Scholar
• Labash C, Avlasevich S, Carlson K, et al. (2016). Mouse Pig-a and micronucleus assays respond to N-ethyl-N-nitrosourea, benzo[a]pyrene, and ethyl carbamate, but not pyrene or methyl carbamate. Environ Mol Mutagen 57:28–40
   PubMed Web of Science ®Google Scholar
• Mathis C, Poussin C, Weisensee D, et al. (2013). Human bronchial epithelial cells exposed in vitro to cigarette smoke at the air–liquid interface resemble bronchial epithelium from human smokers. Am J Physiol 304:L489–503
   Web of Science ®Google Scholar
• Morissette MC, Lamontagne M, Berube JC, et al. (2014). Impact of cigarette smoke on the human and mouse lungs: a gene-expression comparison study. PLoS One 9:e92498
   PubMed Web of Science ®Google Scholar
• Neilson L, Mankus C, Thorne D, et al. (2015). Development of an in vitro cytotoxicity model for aerosol exposure using 3D reconstructed human airway tissue; application for assessment of e-cigarette aerosol. Toxicol In Vitro 29:1952–62
   PubMed Web of Science ®Google Scholar
• OECD (2009). Test guideline 413: subchronic inhalation toxicity: 90-day study. France: OECD Publishing. Available from: http://www.oecd-ilibrary.org/environment/test-no-413-subchronic-inhalation-toxicity-90-day-study_9789264070806-en. [Last accessed: 27 Apr 2016]
   Google Scholar
• OECD (2014). Test guideline 474: mammalian erythrocyte micronucleus test. France: OECD Publishing
   Google Scholar
• Phillips B, Esposito M, Verbeeck J, et al. (2015). Toxicity of aerosols of nicotine and pyruvic acid (separate and combined) in Sprague-Dawley rats in a 28-day OECD 412 inhalation study and assessment of systems toxicology. Inhal Toxicol 27:405–31
   PubMed Web of Science ®Google Scholar
• Piade JJ, Roemer E, Dempsey R, et al. (2014). Toxicological assessment of kretek cigarettes. Part 3: kretek and American-blended cigarettes, inhalation toxicity. Regul Toxicol Pharmacol 70:S26–40
   PubMed Web of Science ®Google Scholar
• Potts RJ, Meckley DR, Shreve WK, et al. (2007). Comparative 13-week inhalation study of cigarette smoke from cigarettes containing cast sheet tobacco. Inhal Toxicol 19:701–24
   PubMed Web of Science ®Google Scholar
• Renne RA, Gideon KM. (2006). Types and patterns of response in the larynx following inhalation. Toxicol Pathol 34:281–5
   PubMed Web of Science ®Google Scholar
• Renne RA, Gideon KM, Miller RA, et al. (1992). Histologic methods and interspecies variations in the laryngeal histology of F344/N rats and B6C3F1 mice. Toxicol Pathol 20:44–51
   PubMed Web of Science ®Google Scholar
• Renne RA, Sagartz JW, Burger GT. (1993). Interspecies variations in the histology of toxicologically-important areas in the larynges of CRL:CD rats and Syrian golden hamsters. Toxicol Pathol 21:542–6
   PubMed Web of Science ®Google Scholar
• Rodgman A, Perfetti TA. 2013. The chemical components of tobacco and tobacco smoke. 2nd ed. Boca Raton, FL: CRC Press
   Google Scholar
• Roemer E, Schramke H, Weiler H, et al. (2014). Mainstream smoke chemistry and in vitro and in vivo toxicity of the reference cigarettes 3R4F and 2R4F. Contrib Tobacco Res 25:316–35
   Google Scholar
• Schramke H, Roemer E, Dempsey R, et al. (2014). Toxicological assessment of kretek cigarettes. Part 7: the impact of ingredients added to kretek cigarettes on inhalation toxicity. Regul Toxicol Pharmacol 70:S81–9
   PubMed Web of Science ®Google Scholar
• Smith CC, O’Donovan MR, Martin EA. (2006). hOGG1 recognizes oxidative damage using the comet assay with greater specificity than FPG or ENDOIII. Mutagenesis 21:185–90
   PubMed Web of Science ®Google Scholar
• Stankowski LF Jr, Aardema MJ, Lawlor TE, et al. (2015). Integration of Pig-a, micronucleus, chromosome aberration and Comet assay endpoints in a 28-day rodent toxicity study with urethane. Mutagenesis 30:335–42
   PubMed Web of Science ®Google Scholar
• Talikka M, Kostadinova R, Xiang Y, et al. (2014). The response of human nasal and bronchial organotypic tissue cultures to repeated whole cigarette smoke exposure. Int J Toxicol 33:506–17
   PubMed Web of Science ®Google Scholar
• Thorne D, Wilson J, Kumaravel TS, et al. (2009). Measurement of oxidative DNA damage induced by mainstream cigarette smoke in cultured NCI-H292 human pulmonary carcinoma cells. Mutat Res 673:3–8
   PubMed Web of Science ®Google Scholar
• Tsuda S, Matsusaka N, Ueno S, et al. (2000). The influence of antioxidants on cigarette smoke-induced DNA single-strand breaks in mouse organs: a preliminary study with the alkaline single cell gel electrophoresis assay. Toxicol Sci 54:104–9
   PubMed Web of Science ®Google Scholar
• UK Committee on Mutagenicity (2011). Guidance on a strategy for genotoxicity testing of chemical substances. United Kingdom: UK Committee on Mutagenicity. Available from: https://www.gov.uk/government/uploads/system/uploads/attachment_data/file/315800/in_vivo_testing_of_genotoxicity_of_chemicals.pdf. [Last accessed: 27 Apr 2016]
   Google Scholar
• Van-Miert E, Vanscheeuwijck P, Meurrens K, et al. (2008). Evaluation of the micronucleus assay in bone marrow and peripheral blood of rats for the determination of cigarette mainstream-smoke activity. Mutat Res 652:131–8
   PubMed Web of Science ®Google Scholar
• Walker D. (1983). Histopathology of the nasal cavity in laboratory animals exposed to cigarette smoke and other irritants. In: Reznik G, Stinson SF. (eds.) Nasal tumors in animals and man. Boca Raton, FL: CRC Press, 115–35
   Google Scholar
• Walker D, Wilton LV, Binns R. (1978a). Inhalation toxicity studies on cigarette smoke (VI). 6-Week comparative experiments using modified flue-cured cigarettes: histopathology of the lung. Toxicology 10:229–40
   PubMed Web of Science ®Google Scholar
• Walker D, Wilton LV, Binns R. (1978b). Inhalation toxicity studies on cigarette smoke (VII). 6-Week comparative experiments using modified flue-cured cigarettes: histopathology of the conducting airways. Toxicology 10:241–59
   PubMed Web of Science ®Google Scholar
• Weber S, Hebestreit M, Wilms T, et al. (2013). Comet assay and air–liquid interface exposure system: a new combination to evaluate genotoxic effects of cigarette whole smoke in human lung cell lines. Toxicol In Vitro 27:1987–91
   PubMed Web of Science ®Google Scholar
• Werley MS, Jerome AM, DeSoi DJ, et al. (2013). A comprehensive evaluation of the toxicology of experimental cigarettes manufactured with banded papers. Inhal. Toxicol 25:19–33
   PubMed Web of Science ®Google Scholar
• Young JT. (1981). Histopathologic examination of the rat nasal cavity. Fundam Appl Toxicol 1:309–12
   PubMedGoogle Scholar
• Zhang S, Xu N, Nie J, et al. (2008). Proteomic alteration in lung tissue of rats exposed to cigarette smoke. Toxicol Lett 178:191–6
   PubMed Web of Science ®Google Scholar