Lung carcinogenicity of inhaled multi-walled carbon nanotube in rats

Particle and Fibre Toxicology

Volumn 13, Issue 1, 2016, Pages

  Kasai, Tatsuya ^a   Umeda, Yumi ^a   Ohnishi, Makoto ^a   Mine, Takashi ^a   Kondo, Hitomi ^a   Takeuchi, Tetsuya ^a   Matsumoto, Michiharu ^a   Fukushima, Shoji ^a  

^a NATIONAL INSTITUTE OF OCCUPATIONAL SAFETY AND HEALTH   (Japan)

Author keywords

Inhalation carcinogenicity; Lung carcinogenicity; Lung carcinoma; Multi walled carbon nanotube; MWCNT; MWNT 7; Rat; Whole body inhalation

Indexed keywords

MULTI WALLED NANOTUBE; CARBON NANOTUBE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRONCHOALVEOLAR LAVAGE FLUID; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; FEMALE; LUNG CARCINOGENESIS; LUNG CARCINOMA; LUNG WEIGHT; MALE; NANOTOXICOLOGY; NONHUMAN; PERITONEUM; PLEURA; PRIORITY JOURNAL; RAT; TOXIC INHALATION; ANIMAL; BODY WEIGHT; CHEMICALLY INDUCED; DRUG EFFECTS; EXPOSURE; FISCHER 344 RAT; LUNG TUMOR; ORGAN SIZE; PATHOLOGY;

ANIMALS; BODY WEIGHT; BRONCHOALVEOLAR LAVAGE FLUID; FEMALE; INHALATION EXPOSURE; LUNG NEOPLASMS; MALE; NANOTUBES, CARBON; ORGAN SIZE; RATS; RATS, INBRED F344;

EID: 84992077691     PISSN: None     EISSN: 17438977     Source Type: Journal    
DOI: 10.1186/s12989-016-0164-2     Document Type: Article

References (65)

1. Endo M. Grow carbon fibers in the vapor phase. In: CHEMTECH. American Chemical Society. 1988. http://www.kroto.info/wp-content/uploads/2015/10/2.Chemtech1988.pdf. Accessed 2 Mar 2016.
2. Rittinghausen S, Hackbarth A, Creutzenberg O, Ernst H, Heinrich U, Leonhardt A, et al. The carcinogenic effect of various multi-walled carbon nanotubes (MWCNTs) after intraperitoneal injection in rats. Part Fiber Toxicol. 2014; doi: 10.1186/s12989-014-0059-z.
3. Mercer RR, Scabilloni JF, Hubbs AF, Wang L, Battelli LA, McKinney W, et al. Extrapulmonary transport of MWCNT following inhalation exposure. Part Fibre Toxicol. 2013; doi: 10.1186/1743-8977-10-38.
4. Stanton MF, Layard M, Tegeris A, Miller E, May M, Morgan E, et al. Relation of particle dimension to carcinogenicity in amphibole asbestoses and other fibrous minerals. J Natl Cancer Inst. 1981;67:965-75.
5. Mcdonald JC, Armstrong B, Case B, Doell D, McGaughey WTE, Mcdonald AD, et al. Mesothelioma and asbestos fiber type. Evidence from lung tissue analyses. Cancer. 1989;63:1544-7.
6. Donaldson K, Murphy FA, Duffin R, Poland DC. Asbestos, carbon nanotubes and the pleural mesothelium: a review of the hypothesis regarding the role of long fibre retention in the parietal pleura, inflammation and mesothelioma. Part Fibre Toxicol. 2010; doi: 10.1186/1743-8977-7-5.
7. Henderson DW, Jones ML, de Klerk N. After Helsinki: a multidisciplinary review of the relationship between asbestos exposure and lung cancer, with emphasis on studies published during 1997-2004. Pathology. 2004;36:517-50.
8. Tomatis L, Cantoni S, Carnevale F, Merler E, Mollo F, Ricci P, et al. The role of asbestos fiber dimensions in the prevention of mesothelioma. Int J Occup Environ Health. 2007;13:64-9.
9. Boulanger G, Andujar P, Pairon JC, Billon-Galland MA, Dion C, Dumortier P, et al. Quantification of short and long asbestos fibers to assess asbestos exposure: a review of fiber size toxicity. Environ Health. 2014; doi: 10.1186/1476-069X-13-59.
10. Poland CA, Duffin R, Kinloch I, Maynard A, Wallace WAH, Seaton A, et al. Carbon nanotubes introduced into the abdominal cavity of mice show asbestos-like pathogenicity in a pilot study. Nature Nanotechnol. 2008;3:423-8.
11. Takagi A, Hirose A, Nishimura T, Fukumori N, Ogata A, Ohashi N, et al. Induction of mesothelioma in p53+/- mouse by intraperitoneal application of multi-wall carbon nanotube. J Toxicol Sci. 2008;33:105-16.
12. Sakamoto Y, Nakae D, Fukumori N, Tayama K, Maekawa A, Imai K, et al. Induction of mesothelioma by a single intrascrotal administration of multi-wall carbon nanotube in intact male Fischer 344 rats. J Toxicol Sci. 2009;34:65-76.
13. Nagai H, Okazaki Y, Chew SH, Misawa N, Yamashita Y, Akatsuka S, et.al. Diameter and rigidity of multiwalled carbon nanotubes are critical factors in mesothelial injury and carcinogenesis. PNAS. 2011; doi: 10.1073/pnas.1110013108.
14. Takagi A, Hirose A, Futakuchi M, Tsukada H, Kanno J. Dose-dependent mesothelioma induction by intraperitoneal administration of multi-wall carbon nanotubes in p53 heterozygous mice. Cancer Sci. 2012;103:1440-4.
15. Dahm MM, Schubauer-Berigan MK, Evans DE, Birch ME, Fernback JE, Deddens JA. Carbon nanotube and nanofiber exposure assessments: an analysis of 14 site visits. Ann Occup Hyg. 2015;59:705-23.
16. Takaya M, Serita F, Ono-Ogasawara M, Shinohara Y, Saito H, Koda S. Airborne particles in a multi-wall carbon nanotube production plant: Observation of particle emission and personal exposure I: Measurement in the packing process. JPN J Ind Health (San Ei Shi). 2010;52:182-8 (In Japanese).
17. Ryman-Rasmussen JP, Cesta MF, Brody AR, Shipley-Phillips JK, Everitt JI, Tewksbury EW, et al. Inhaled carbon nanotubes reach the subpleural tissue in mice. Nature Nanotechnol. 2009;4:747-51.
18. Poter DW, Hubbs AF, Chen TB, McKinny W, Mercer RR, Wolfarth MG, et al. Acute pulmonary dose-responses to inhaled multiwalled carbon nanotubes. Nanotoxicology. 2012;7:1179-94.
19. Sargent LM, Porter DW, Staska LM, Hubbs AF, Lowry DT, Battelli L, et al. Promotion of lung adenocarcinoma following inhalation exposure to multi-walled carbon nanotubes. Part Fibre Toxicol. 2014; doi: 10.1186/1743-8977-11-3.
20. Kasai T, Gotoh K, Nishizawa T, Sasaki T, Katagiri T, Umeda Y, et al. Development of a new multi-walled carbon nanotube (MWCNT) aerosol generation and exposure system and confirmation of suitability for conducting a single-exposure inhalation study of MWCNT in rats. Nanotoxicology. 2014;8:169-78.
21. Umeda Y, Kasai T, Saito M, Kondo H, Toya T, Aiso S, et al. Two-week toxicity of multi-walled carbon nanotubes by whole-body inhalation exposure in rats. J Toxicol Pathol. 2013;26:131-40.
22. Kasai T, Umeda Y, Ohnishi M, Kondo H, Takeuchi T, Aiso S, et al. Thirteen-week study of toxicity of fiber-like multi-walled carbon nanotubes with whole-body inhalation exposure in rats. Nanotoxicology. 2015;9:413-22.
23. Organisation for Economic Cooperation and Development. OECD guideline for testing of chemicals 451 "Carcinogenicity Studies." Adopted September 2009. Paris: OECD; 2009.
24. McInnes EF, Miller RA. A review of upper respiratory tract inhalation pathology. Comparative Clinic Path. 2007;16:215-22.
25. Dungworth DL, Ernst H, Nolte T, More U. Nonneoplastic lesions in the lung. In: Mohr U, Dungworth DL, Capen CC, editors. Pathology of the aging rats, vol. 1. Washington DC: ILSI press; 1992. p. 143-60.
26. Renne R, Brix A, Harkema J, Herbert R, Kittel B, Lewis D, et al. Proliferative and nonproliferative lesions of the rat and mouse respiratory tract. Toxicol Pathol. 2009;37:5S-73S.
27. Dungworth DL, Hahn FF, Nikula KJ. Noncarcinogenic responses of the respiratory tract to inhaled toxicants. In: McClellan RO, Henderson RF, editors. Concepts in inhalation toxicology. 2nd ed. Washington DC: Taylor & Francis; 1995. p. 533-76.
28. Bannasch P, Griesemer RA, Anders F, Becker R, Cabral JR, Della PG, et al. Long-term assays for carcinogenicity in animals. In: Montesano R, Bartsch H, Vainio H, Wilbourn J, Yamasaki H, editors. Long-term and short-term assays for carcinogens: A critical appraisal, 83. Lyon: IARC Scientific Publications; 1986. p. 13-83.
29. Sontag JM, Page NP, Saffiotti U. Guidelines for carcinogen bioassay in small rodents: NCI-CG-TR-1. Washington DC: DHEW; 1976.
30. Donaldson K, Poland CA, Murphy FA, MacFarlane M, Chermova T, Schinwald A. Pulmonary toxicity of carbon nanotubes and asbestos - similarities and differences. Adv Drug Deliv Rev. 2013;65:2078-86.
31. Muller J, Delos M, Panin N, Rabolli V, Huaux F, Lison D. Absence of carcinogenic response to multi-wall carbon nanotubes in a 104-week bioassay in the peritoneal cavity of the rat. Toxicol Sci. 2009;110:442-8.
32. Bide RW, Armour SJ, Yee E. Allometric respiration/body mass data for animals to be used for estimates of inhalation toxicity to young adult humans. J Appl Toxicol. 2000;20:273-90.
33. Kuempel ED. Carbon nanotube risk assessment: implications for exposure and medical monitoring. J Occup Environ Med. 2011;53:S91-7.
34. Erdely A, Dahm M, Chen BT, Zeidler-Erdely PC, Fernback JE, Birch ME, et al. Carbon nanotube dosimetry: from workplace exposure assessment to inhalation toxicology. Part Fibre Toxicol. 2013; doi: 10.1186/1743-8977-10-53.
35. Han JH, Lee EJ, Lee JH, So KP, Lee YH, Bae GN, et al. Monitoring multiwalled carbon nanotube exposure in carbon nanotube research facility. Inhal Toxicol. 2008;20:741-9.
36. Lee JH, Lee SB, Bae GN, Jeon KS, Yoon JU, Ji JH, et al. Exposure assessment of carbon nanotube manufacturing workplaces. Inhal Toxicol. 2010;22:369-81.
37. Maynard AD, Baron PA, Foley M, Shvedova AA, Kisin ER, Castranova V. Exposure to carbon nanotube material: aerosol release during the handling of unrefined single-walled carbon nanotube material. J Toxicol Environ Health A. 2004;67:87-107.
38. Pulskamp K, Diabate S, Krug HF. Carbon nanotubes show no sign of acute toxicity but induce intracellular reactive oxygen species in dependence on contaminants. Toxicol Lett. 2007;168:58-74.
39. Sohaebuddin SK, Thevenot PT, Baker D, Eaton JW, Tang L. Nanomaterial cytotoxicity is composition, size, and cell type dependent. Part Fibre Toxicol. 2010; doi: 10.1186/1743-8977-7-22.
40. Xu J, Futakuchi M, Iigo M, Fukamachi K, Alexander DB, Shimizu H, et al. Involvement of macrophage inflammatory protein 1a (MIP1a) in promotion of rat lung and mammary carcinogenic activity of nanoscale titanium dioxide particles administered by intra-pulmonary spraying. Carcinogenesis. 2010;31:927-35.
41. Ma-Hock L, Strauss V, Treumann S, Küttler K, Wohlleben W, Hofmann T, et al. Comparative inhalation toxicity of multi-wall carbon nanotubes, graphene, graphite nanoplatelets and low surface carbon black. Part Fibre Toxicol. 2013; doi: 10.1186/1743-8977-10-23.
42. Mauderly JL. Relevance of particle-induced rat lung tumors for assessing lung carcinogenic hazard and human lung cancer risk. Environ Health Perspect. 1997;105:1337-46.
43. Reeves AL, Puro HE, Smith RG, Vorwald AJ. Experimental asbestos carcinogenesis. Environ Res. 1971;4:496-511.
44. Yee H, Yie TA, Goldberg J, Wong KM, Rom WN. Immunohistochemical study of fibrosis and adenocarcinoma in dominant-negative p53 transgenic mice exposed to chrysotile asbestos and benzo(a)pyrene. J Environ Pathol Toxicol Oncol. 2008;27:267-76.
45. Suzui M, Futakuchi M, Fukamachi K, Numano T, Abdelgied M, Takahashi S, et al. Multiwalled carbon nanotubes intratracheally instilled into the rat lung induce development of pleural malignant mesothelioma and lung tumors. Cancer Sci. 2016; doi: 10.1111/cas.12954.
46. Davis JM, Addison J, Bolton RE, Donaldson K, Jones AD, Smith T. The pathogenicity of long versus short fibre samples of amosite asbestos administered to rats by inhalation and intraperitoneal injection. Br J Exp Pathol. 1986;67:415-30.
47. Davis JM, Jones AD. Comparisons of the pathogenicity of long and short fibres of chrysotile asbestos in rats. Br J Exp Pathol. 1988;69:717-37.
48. Mossman BT, Lippmann M, Hesterberg TW, Kelsey KT, Barchowsky A, Bonner JC. Pulmonary end points (lung carcinomas and asbestosis) following inhalation exposure to asbestos. J Toxicol Env Heal B. 2011;14:76-121.
49. Ema M, Imamura T, Suzuki H, Kobayashi N, Naya M, Nakanishi J. Evaluation of genotoxicity of multi-walled carbon nanotubes in a battery of in vitro and in vivo assays. Reg Toxi Pharm. 2012;63(2):188-95.
50. Asakura M, Sugiyama T, Sasaki T, Takaya M, Koda S, Nagano K, et al. Cytotoxicity and mutagenicity of multi-wall carbon nanotubes in cultured Chinese hamster lung cells. J Occup Health. 2010;52:155-66.
51. Yasui M, Kamoshita N, Nishimura T, Honma M. Mechanism of induction of binucleated cells by multiwalled carbon nanotubes as revealed by live-cell imaging analysis. Genes Environ. 2015; doi: 10.1186/s41021-015 - 0003-y.
52. Kato T, Totsuka Y, Ishino K, Matsumoto Y, Tada Y, Nakae D, et al. Genotoxicity of multi-walled carbon nanotubes in both in vitro and in vivo assay systems. Nanotoxicology. 2013;7:452-61.
53. Benbrahim-Tallaa L, Guha N, Bouvard V, Carel R, Ghissassi F El, Grosse Y, et al. Carcinogenicity of fluoro-edenite, silicon carbide fibres and whiskers, and carbon nanotubes. Lancet Oncol. 2014. http://impactitalia.gov.it/binary/pres/cont/111_Grosse_nanotubes.pdf.
54. National Institute for Occupational Safety and Health (NIOSH). Current intelligence bulletin 65. Occupational exposure to carbon nanotubes and nanofibers. US Department of Health and Human Services Centers for Disease Control and Prevention, DHHS (NIOSH) Pub. No. 2013-145. Cincinnati: NIOSH; 2013. https://www.cdc.gov/niosh/docs/2013-145/pdfs/2013-145.pdf.
55. United States Environmental Protection Agency (US.EPA). Benchmark dose software version 2.6 user's manual. EPA/100/R-12/001. Washington, DC: US EPA; 2015.
56. Bolt HM, Degen GH. Human carcinogenic risk evaluation, part II: contributions of the EUROTOX specialty section for carcinogenesis. Toxico Sci. 2004;81:3-6.
57. Fukushima S, Wei M, Kakehashi A, Wnibuchi H. Threshold for genotoxic carcinogen: evidence from mechanism-based carcinogenicity studies. Cancer risk assessment. 2010. doi: 10.1002/9780470622728.ch8.
58. Takaya M, Serita F, Yamazaki K, Aiso S, Kubota H, Asakura M, et al. Characteristics of multiwall carbon nanotubes for an intratracheal instillation study with rats. Ind Health. 2010;48:452-9.
59. Organisation for Economic Cooperation and Development. OECD principles of good laboratory practice. Adopted 1981. Paris: OECD; 1981.
60. Nagano K, Katagiri T, Aiso S, Senoh H, Sakura Y, Takeuchi T. Spontaneous lesions of nasal cavity in aging F344 rats and BDF1 mice. Exp Toxicol Pathol. 1997;49:97-104.
61. Kohyama N, Suzuki Y. Analysis of asbestos fibers in lung parenchyma, pleural plaques, and mesothelioma tissues of North American insulation workers. Ann NY Acad Sci. 1991;643:27-52.
62. Ohnishi M, Yajima H, Kasai T, Umeda Y, Yamamoto M, Yamamoto S, et al. Novel method using hybrid markers: development of an approach for pulmonary measurement of multi-walled carbon nanotubes. J Occup Med Toxicol. 2013; doi: 10.1186/1745-6673-8-30.
63. Peto R, Pike MC, Day NE, Gray RG, Lee PN, Parish S, et al. Annex Guidelines for simple, sensitive significance tests for carcinogenic effects in long-term animal experiments: Long-term and short-term screening assays for carcinogens: a critical appraisal. IARC Monographs 1980; Suppl 2:311-426.
64. Kaplan EL, Meier P. Nonparametric estimation from incomplete observations. Am Stat Assoc J. 1958;53:457-81.
65. Peto R, Pike MC, Armitage P, Breslow NE, Cox DR, Howard SV, et al. Design and analysis of randomized clinical trials requiring prolonged observation of each patient. II. Analysis examples. Br J Cancer. 1977;35:1-39.