Grouping MWCNTs based on their similar potential to cause pulmonary hazard after inhalation: a case-study
Tóm tắt
The EU-project GRACIOUS developed an Integrated Approach to Testing and Assessment (IATA) to support grouping high aspect ratio nanomaterials (HARNs) presenting a similar inhalation hazard. Application of grouping reduces the need to assess toxicity on a case-by-case basis and supports read-across of hazard data from substances that have the data required for risk assessment (source) to those that lack such data (target). The HARN IATA, based on the fibre paradigm for pathogenic fibres, facilitates structured data gathering to propose groups of similar HARN and to support read-across by prompting users to address relevant questions regarding HARN morphology, biopersistence and inflammatory potential. The IATA is structured in tiers, allowing grouping decisions to be made using simple in vitro or in silico methods in Tier1 progressing to in vivo approaches at the highest Tier3. Here we present a case-study testing the applicability of GRACIOUS IATA to form an evidence-based group of multiwalled carbon nanotubes (MWCNT) posing a similar predicted fibre-hazard, to support read-across and reduce the burden of toxicity testing. The case-study uses data on 15 different MWCNT, obtained from the published literature. By following the IATA, a group of 2 MWCNT was identified (NRCWE006 and NM-401) based on a high degree of similarity. A pairwise similarity assessment was subsequently conducted between the grouped MWCNT to evaluate the potential to conduct read-across and fill data gaps required for regulatory hazard assessment. The similarity assessment, based on expert judgement of Tier 1 assay results, predicts both MWCNT are likely to cause a similar acute in vivo hazard. This result supports the possibility for read-across of sub-chronic and chronic hazard endpoint data for lung fibrosis and carcinogenicity between the 2 grouped MWCNT. The implications of accepting the similarity assessment based on expert judgement of the MWCNT group are considered to stimulate future discussion on the level of similarity between group members considered sufficient to allow regulatory acceptance of a read-across argument. This proof-of-concept case-study demonstrates how a grouping hypothesis and IATA may be used to support a nuanced and evidence-based grouping of ‘similar’ MWCNT and the subsequent interpolation of data between group members to streamline the hazard assessment process.
Tài liệu tham khảo
Stone V, Gottardo S, Bleeker EAJ, Braakhuis H, Dekkers S, Fernandes T, Haase A, Hunt N, Hristozov D, Jantunen P, Jeliazkova N, Johnston H, Lamon L, Murphy F, Rasmussen K, Rauscher H, Jiménez AS, Svendsen C, Spurgeon D, Oomen AG. A framework for grouping and read-across of nanomaterials- supporting innovation and risk assessment. Nano Today. 2020;35:100941. https://doi.org/10.1016/j.nantod.2020.100941.
ECHA (2013) Grouping of substances and read-across approach, Part 1: Introductory note. 1–11.
Fadeel B, Kostarelos K. Grouping all carbon nanotubes into a single substance category is scientifically unjustified. Nat Nanotechnol. 2020;15(3):164. https://doi.org/10.1038/s41565-020-0654-0.
OECD. (2018a). Test No. 412: Subacute inhalation toxicity: 28-day study. OECD. https://doi.org/10.1787/9789264070783-en.
OECD. (2018b). Test No. 413: Subchronic inhalation toxicity: 90-day Study. OECD. https://doi.org/10.1787/9789264070806-en
Braakhuis HM, Murphy F, Ma-Hock L, Dekkers S, Keller J, Oomen AG, Stone V. An integrated approach to testing and assessment to support grouping and read-across of nanomaterials after inhalation exposure. Appl Vitro Toxicol. 2021;7(3):112–28. https://doi.org/10.1089/aivt.2021.0009.
Murphy F, Dekkers S, Braakhuis H, Ma-Hock L, Johnston H, Janer G, di Cristo L, Sabella S, Jacobsen NR, Oomen AG, Haase A, Fernandes T, Stone V. An integrated approach to testing and assessment of high aspect ratio nanomaterials and its application for grouping based on a common mesothelioma hazard. NanoImpact. 2021. https://doi.org/10.1016/j.impact.2021.100314.
Donaldson K, Murphy FA, Duffin R, Poland CA. 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;7(1):5. https://doi.org/10.1186/1743-8977-7-5.
Yang H, Testa JR, Carbone M. Mesothelioma epidemiology, carcinogenesis, and pathogenesis. Curr Treat Options Oncol. 2008;9(2–3):147–57. https://doi.org/10.1007/s11864-008-0067-z.
Di Ianni E, Erdem JS, Møller P, Sahlgren NM, Poulsen SS, Knudsen KB, Zienolddiny S, Saber AT, Wallin H, Vogel U, Jacobsen NR. In vitro-in vivo correlations of pulmonary inflammogenicity and genotoxicity of MWCNT. Part Fibre Toxicol. 2021;18(1):25. https://doi.org/10.1186/s12989-021-00413-2.
Jackson P, Kling K, Jensen KA, Clausen PA, Madsen AM, Wallin H, Vogel U. Characterization of genotoxic response to 15 multiwalled carbon nanotubes with variable physicochemical properties including surface functionalizations in the FE1-Muta(TM) mouse lung epithelial cell line. Environ Molecul Mutagenes. 2015;56(2):183–203. https://doi.org/10.1002/em.21922.
Knudsen KB, Berthing T, Jackson P, Poulsen SS, Mortensen A, Jacobsen NR, Skaug V, Szarek J, Hougaard KS, Wolff H, Wallin H, Vogel U. Physicochemical predictors of multi-walled carbon nanotube–induced pulmonary histopathology and toxicity one year after pulmonary deposition of 11 different multi-walled carbon nanotubes in mice. Basic Clin Pharmacol Toxicol. 2019;124(2):211–27. https://doi.org/10.1111/bcpt.13119.
Poulsen SS, Jackson P, Kling K, Knudsen KB, Skaug V, Kyjovska ZO, Thomsen BL, Clausen PA, Atluri R, Berthing T, Bengtson S, Wolff H, Jensen KA, Wallin H, Vogel U. Multi-walled carbon nanotube physicochemical properties predict pulmonary inflammation and genotoxicity. Nanotoxicology. 2016;10(9):1263–75. https://doi.org/10.1080/17435390.2016.1202351.
Jeliazkova N, Bleeker E, Cross R, Haase A, Janer G, Peijnenburg W, Pink M, Rauscher H, Svendsen C, Tsiliki G, Zabeo A, Hristozov D, Stone V, Wohlleben W. How can we justify grouping of nanoforms for hazard assessment? Concepts and tools to quantify similarity. NanoImpact. 2022;25:100366. https://doi.org/10.1016/j.impact.2021.100366.
Gaté L, Knudsen KB, Seidel C, Berthing T, Chézeau L, Jacobsen NR, Valentino S, Wallin H, Bau S, Wolff H, Sébillaud S, Lorcin M, Grossmann S, Viton S, Nunge H, Darne C, Vogel U, Cosnier F. Pulmonary toxicity of two different multi-walled carbon nanotubes in rat: Comparison between intratracheal instillation and inhalation exposure. Toxicol Appl Pharmacol. 2019;375:17–31. https://doi.org/10.1016/j.taap.2019.05.001.
Kasai T, Gotoh K, Nishizawa T, Sasaki T, Katagiri T, Umeda Y, Toya T, Fukushima S. 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(2):169–78. https://doi.org/10.3109/17435390.2013.766277.
Mercer RR, Scabilloni JF, Hubbs AF, Battelli LA, McKinney W, Friend S, Wolfarth MG, Andrew M, Castranova V, Porter DW. Distribution and fibrotic response following inhalation exposure to multi-walled carbon nanotubes. Part Fibre Toxicol. 2013;10:33. https://doi.org/10.1186/1743-8977-10-33.
Kasai T, Umeda Y, Ohnishi M, Kondo H, Takeuchi T, Aiso S, Nishizawa T, Matsumoto M, Fukushima S. Thirteen-week study of toxicity of fiber-like multi-walled carbon nanotubes with whole-body inhalation exposure in rats. Nanotoxicology. 2015;9(4):413–22. https://doi.org/10.3109/17435390.2014.933903.
Kasai T, Umeda Y, Ohnishi M, Mine T, Kondo H, Takeuchi T, Matsumoto M, Fukushima S. Lung carcinogenicity of inhaled multi-walled carbon nanotube in rats. Part Fibre Toxicol. 2016;13(1):53. https://doi.org/10.1186/s12989-016-0164-2.
Umeda Y, Kasai T, Saito M, Kondo H, Toya T, Aiso S, Okuda H, Nishizawa T, Fukushima S. Two-week Toxicity of Multi-walled Carbon Nanotubes by Whole-body Inhalation Exposure in Rats. J Toxicol Pathol. 2013;26(2):131–40. https://doi.org/10.1293/tox.26.131.
Osmond-McLeod MJ, Poland CA, Murphy F, Waddington L, Morris H, Hawkins SC, Clark S, Aitken R, McCall MJ, Donaldson K. Durability and inflammogenic impact of carbon nanotubes compared with asbestos fibres. Part Fibre Toxicol. 2011;8:15. https://doi.org/10.1186/1743-8977-8-15.
Arts JHE, Irfan M-A, Keene AM, Kreiling R, Lyon D, Maier M, Michel K, Neubauer N, Petry T, Sauer UG, Warheit D, Wiench K, Wohlleben W, Landsiedel R. Case studies putting the decision-making framework for the grouping and testing of nanomaterials (DF4nanoGrouping) into practice. Regulatory Toxicol Pharmacol. 2016;76:234–61. https://doi.org/10.1016/j.yrtph.2015.11.020.
Nagai H, Okazaki Y, Chew SH, Misawa N, Yamashita Y, Akatsuka S, Ishihara T, Yamashita K, Yoshikawa Y, Yasui H, Jiang L, Ohara H, Takahashi T, Ichihara G, Kostarelos K, Miyata Y, Shinohara H, Toyokuni S. Diameter and rigidity of multiwalled carbon nanotubes are critical factors in mesothelial injury and carcinogenesis. Proc Nat Acad Sci. 2011;108(49):1330–8. https://doi.org/10.1073/pnas.1110013108.
Porter DW, Hubbs AF, Mercer RR, Wu N, Wolfarth MG, Sriram K, Leonard S, Battelli L, Schwegler-Berry D, Friend S, Andrew M, Chen BT, Tsuruoka S, Endo M, Castranova V. Mouse pulmonary dose- and time course-responses induced by exposure to multi-walled carbon nanotubes. Toxicology. 2010;269(2):136–47. https://doi.org/10.1016/j.tox.2009.10.017.
Takagi A, Hirose A, Nishimura T, Fukumori N, Ogata A, Ohashi N, Kitajima S, Kanno J. Induction of mesothelioma in p53+/− mouse by intraperitoneal application of multi-wall carbon nanotube. J Toxicol Sci. 2008;33(1):105–16. https://doi.org/10.2131/jts.33.105.
Murphy FA, Poland CA, Duffin R, Donaldson K. Length-dependent pleural inflammation and parietal pleural responses after deposition of carbon nanotubes in the pulmonary airspaces of mice. Nanotoxicology. 2012;7(6):1157–67. https://doi.org/10.3109/17435390.2012.713527.
Murphy FA, Schinwald A, Poland CA, Donaldson K. The mechanism of pleural inflammation by long carbon nanotubes: interaction of long fibres with macrophages stimulates them to amplify pro-inflammatory responses in mesothelial cells. Part Fibre Toxicol. 2012;9(1):8. https://doi.org/10.1186/1743-8977-9-8.
Palomäki J, Välimäki E, Sund J, Vippola M, Clausen PA, Jensen KA, Savolainen K, Matikainen S, Alenius H. Long, needle-like carbon nanotubes and asbestos activate the NLRP3 inflammasome through a similar mechanism. ACS Nano. 2011;5(9):6861–70. https://doi.org/10.1021/nn200595c.
Købler C, Poulsen SS, Saber AT, Jacobsen NR, Wallin H, Yauk CL, Halappanavar S, Vogel U, Qvortrup K, Mølhave K. Time-dependent subcellular distribution and effects of carbon nanotubes in lungs of mice. PLoS ONE. 2015;10(1):e0116481–e0116481. https://doi.org/10.1371/journal.pone.0116481.
Morimoto Y, Kobayashi N. Evaluations of the carcinogenicity of carbon nanotubes, fluoro-edinite, and silicon carbide by the international agency for research on cancer (IARC). Nihon eiseigaku zasshi. Japanese J Hyg. 2016;71(3):252–9. https://doi.org/10.1265/jjh.71.252.
BSI. (1993). BS EN 481:1993, BS 6069–3.5:1993 Workplace atmospheres. Size fraction definitions for measurement of airborne particles. European Committee for Standardization.
Miller FJ, Asgharian B, Schroeter JD, Price O. Improvements and additions to the multiple path particle dosimetry model. J Aerosol Sci. 2016;99:14–26. https://doi.org/10.1016/j.jaerosci.2016.01.018.
Boyles M, Murphy F, Mueller W, Wohlleben W, Jacobsen NR, Braakhuis H, Giusti A, Stone V. Development of a standard operating procedure for the DCFH2-DA acellular assessment of reactive oxygen species produced by nanomaterials. Toxicol Mech Methods. 2022. https://doi.org/10.1080/15376516.2022.2029656.
Gren L, Malmborg VB, Jacobsen NR, Shukla PC, Bendtsen KM, Eriksson AC, Essig YJ, Krais AM, Loeschner K, Shamun S, Strandberg B, Tunér M, Vogel U, Pagels J. Effect of renewable fuels and intake O2 concentration on diesel engine emission characteristics and reactive oxygen species (ROS) formation. In Atmosphere. 2020. https://doi.org/10.3390/atmos11060641.
Modrzynska J, Berthing T, Ravn-Haren G, Jacobsen NR, Weydahl IK, Loeschner K, Mortensen A, Saber AT, Vogel U. Primary genotoxicity in the liver following pulmonary exposure to carbon black nanoparticles in mice. Part Fibre Toxicol. 2018;15(1):2. https://doi.org/10.1186/s12989-017-0238-9.
Rahman L, Jacobsen NR, Aziz SA, Wu D, Williams A, Yauk CL, White P, Wallin H, Vogel U, Halappanavar S. Multi-walled carbon nanotube-induced genotoxic, inflammatory and pro-fibrotic responses in mice: Investigating the mechanisms of pulmonary carcinogenesis. Mutation Res /Genetic Toxicol Environ Mutagenes. 2017;823:28–44. https://doi.org/10.1016/j.mrgentox.2017.08.005.
Duke KS, Taylor-Just AJ, Ihrie MD, Shipkowski KA, Thompson EA, Dandley EC, Parsons GN, Bonner JC. STAT1-dependent and -independent pulmonary allergic and fibrogenic responses in mice after exposure to tangled versus rod-like multi-walled carbon nanotubes. Part Fibre Toxicol. 2017;14(1):26. https://doi.org/10.1186/s12989-017-0207-3.
Oberdörster G, Kuhlbusch TAJ. In vivo effects: Methodologies and biokinetics of inhaled nanomaterials. NanoImpact. 2018;10:38–60. https://doi.org/10.1016/j.impact.2017.10.007.
Seidel C, Zhernovkov V, Cassidy H, Kholodenko B, Matallanas D, Cosnier F, Gaté L. Inhaled multi-walled carbon nanotubes differently modulate global gene and protein expression in rat lungs. Nanotoxicology. 2021;15(2):238–56. https://doi.org/10.1080/17435390.2020.1851418.
Jagiello K, Halappanavar S, Rybińska-Fryca A, Willliams A, Vogel U, Puzyn T. Transcriptomics-based and AOP-informed structure-activity relationships to predict pulmonary pathology induced by multiwalled carbon nanotubes. Small. 2021;17(15):2003465. https://doi.org/10.1002/smll.202003465.
Mossman BT, Churg A. Mechanisms in the pathogenesis of asbestosis and silicosis. Am J Respir Crit Care Med. 1998;157(5):1666–80. https://doi.org/10.1164/ajrccm.157.5.9707141.
Fraser K, Kodali V, Yanamala N, Birch ME, Cena L, Casuccio G, Bunker K, Lersch TL, Evans DE, Stefaniak A, Hammer MA, Kashon ML, Boots T, Eye T, Hubczak J, Friend SA, Dahm M, Schubauer-Berigan MK, Siegrist K, Erdely A. Physicochemical characterization and genotoxicity of the broad class of carbon nanotubes and nanofibers used or produced in U.S. facilities. Particle Fibre Toxicol. 2020;17(1):62. https://doi.org/10.1186/s12989-020-00392-w.
Aschberger K, Asturiol D, Lamon L, Richarz A, Gerloff K, Worth A. Grouping of multi-walled carbon nanotubes to read-across genotoxicity: A case study to evaluate the applicability of regulatory guidance. Comput Toxicol. 2019;9:22–35. https://doi.org/10.1016/j.comtox.2018.10.001.
Kotzabasaki M, Sotiropoulos I, Charitidis C, Sarimveis H. Machine learning methods for multi-walled carbon nanotubes (MWCNT) genotoxicity prediction. Nanoscale Adv. 2021;3(11):3167–76. https://doi.org/10.1039/D0NA00600A.
Fraser K, Hubbs A, Yanamala N, Mercer RR, Stueckle TA, Jensen J, Eye T, Battelli L, Clingerman S, Fluharty K, Dodd T, Casuccio G, Bunker K, Lersch TL, Kashon ML, Orandle M, Dahm M, Schubauer-Berigan MK, Kodali V, Erdely A. Histopathology of the broad class of carbon nanotubes and nanofibers used or produced in U.S. facilities in a murine model. Particle Fibre Toxicol. 2021;18(1):47. https://doi.org/10.1186/s12989-021-00440-z.
Møller P, Jacobsen NR. Weight of evidence analysis for assessing the genotoxic potential of carbon nanotubes. Crit Rev Toxicol. 2017;47(10):871–88. https://doi.org/10.1080/10408444.2017.1367755.
Møller P, Wils RS, Di Ianni E, Gutierrez CAT, Roursgaard M, Jacobsen NR. Genotoxicity of multi-walled carbon nanotube reference materials in mammalian cells and animals. Mutat Res, Rev Mutat Res. 2021;788: 108393. https://doi.org/10.1016/j.mrrev.2021.108393.
Huaux F, d’Ursel de Bousies V, Parent M-A, Orsi M, Uwambayinema F, Devosse R, Ibouraadaten S, Yakoub Y, Panin N, Palmai-Pallag M, van der Bruggen P, Bailly C, Marega R, Marbaix E, Lison D. Mesothelioma response to carbon nanotubes is associated with an early and selective accumulation of immunosuppressive monocytic cells. Part Fibre Toxicol. 2016;13(1):46. https://doi.org/10.1186/s12989-016-0158-0.
Sakamoto Y, Hojo M, Kosugi Y, Watanabe K, Hirose A, Inomata A, Suzuki T, Nakae D. Comparative study for carcinogenicity of 7 different multi-wall carbon nanotubes with different physicochemical characteristics by a single intraperitoneal injection in male Fischer 344 rats. J Toxicol Sci. 2018;43(10):587–600. https://doi.org/10.2131/jts.43.587.
Sakamoto Y, Nakae D, Fukumori N, Tayama K, Maekawa A, Imai K, Hirose A, Nishimura T, Ohashi N, Ogata A. Induction of mesothelioma by a single intrascrotal administration of multi-wall carbon nanotube in intact male Fischer 344 rats. J Toxicol Sci. 2009;34(1):65–76. https://doi.org/10.2131/jts.34.65.
Abdelgied M, El-Gazzar AM, Alexander WT, Numano T, Iigou M, Naiki-Ito A, Takase H, Hirose A, Taquahashi Y, Kanno J, Abdelhamid M, Abdou KA, Takahashi S, Alexander DB, Tsuda H. Carcinogenic effect of potassium octatitanate (POT) fibers in the lung and pleura of male Fischer 344 rats after intrapulmonary administration. Part Fibre Toxicol. 2019;16(1):34. https://doi.org/10.1186/s12989-019-0316-2.
Numano T, Higuchi H, Alexander DB, Alexander WT, Abdelgied M, El-Gazzar AM, Saleh D, Takase H, Hirose A, Naiki-Ito A, Suzuki S, Takahashi S, Tsuda H. MWCNT-7 administered to the lung by intratracheal instillation induces development of pleural mesothelioma in F344 rats. Cancer Sci. 2019;110(8):2485–92. https://doi.org/10.1111/cas.14121.
Sun B, Wang X, Ji Z, Li R, Xia T. NLRP3 inflammasome activation induced by engineered nanomaterials. Small. 2013;9(9–10):1595–607. https://doi.org/10.1002/smll.201201962.
Wang X, Sun B, Liu S, Xia T. Structure activity relationships of engineered nanomaterials in inducing NLRP3 inflammasome activation and chronic lung fibrosis. NanoImpact. 2017;6:99–108. https://doi.org/10.1016/j.impact.2016.08.002.
Drasler B, Sayre P, Steinhäuser KG, Petri-Fink A, Rothen-Rutishauser B. In vitro approaches to assess the hazard of nanomaterials. NanoImpact. 2017;8:99–116. https://doi.org/10.1016/j.impact.2017.08.002.