The American Journal of Pathology
Volume 178, Issue 6 , Pages 2587-2600, June 2011

Length-Dependent Retention of Carbon Nanotubes in the Pleural Space of Mice Initiates Sustained Inflammation and Progressive Fibrosis on the Parietal Pleura

  • Fiona A. Murphy

      Affiliations

    • University of Edinburgh/Medical Research Council, the Centre for Inflammation Research, Queen's Medical Research Institute, Edinburgh, United Kingdom
  • ,
  • Craig A. Poland

      Affiliations

    • University of Edinburgh/Medical Research Council, the Centre for Inflammation Research, Queen's Medical Research Institute, Edinburgh, United Kingdom
    • Safenano, Institute of Occupational Medicine, Edinburgh, United Kingdom
  • ,
  • Rodger Duffin

      Affiliations

    • University of Edinburgh/Medical Research Council, the Centre for Inflammation Research, Queen's Medical Research Institute, Edinburgh, United Kingdom
  • ,
  • Khuloud T. Al-Jamal

      Affiliations

    • Nanomedicine Laboratory, Centre for Drug Delivery Research, the School of Pharmacy, University of London, London, United Kingdom
    • Department of Pharmacy, the Institute of Pharmaceutical Science, King's College London, London, United Kingdom
  • ,
  • Hanene Ali-Boucetta

      Affiliations

    • Nanomedicine Laboratory, Centre for Drug Delivery Research, the School of Pharmacy, University of London, London, United Kingdom
  • ,
  • Antonio Nunes

      Affiliations

    • Nanomedicine Laboratory, Centre for Drug Delivery Research, the School of Pharmacy, University of London, London, United Kingdom
  • ,
  • Fiona Byrne

      Affiliations

    • School of Physics, the Centre for Research on Adaptive Nanostructures and Nanodevices, Trinity College, Dublin, Ireland
    • School of Medicine, Trinity College, Dublin, Ireland
  • ,
  • Adriele Prina-Mello

      Affiliations

    • School of Physics, the Centre for Research on Adaptive Nanostructures and Nanodevices, Trinity College, Dublin, Ireland
    • School of Medicine, Trinity College, Dublin, Ireland
  • ,
  • Yuri Volkov

      Affiliations

    • School of Physics, the Centre for Research on Adaptive Nanostructures and Nanodevices, Trinity College, Dublin, Ireland
    • School of Medicine, Trinity College, Dublin, Ireland
  • ,
  • Shouping Li

      Affiliations

    • Department of Pharmaceutical Sciences, Center of Excellence for Nanostructured Materials, University of Trieste, Trieste, Italy
  • ,
  • Stephen J. Mather

      Affiliations

    • Department of Nuclear Medicine, St. Bartholomew's Hospital, London, United Kingdom
  • ,
  • Alberto Bianco

      Affiliations

    • CNRS, Institut de Biologie Moléculaire et Cellulaire, Immunologie et Chimie Thérapeutiques, Strasbourg, France
  • ,
  • Maurizio Prato

      Affiliations

    • Department of Pharmaceutical Sciences, Center of Excellence for Nanostructured Materials, University of Trieste, Trieste, Italy
  • ,
  • William MacNee

      Affiliations

    • University of Edinburgh/Medical Research Council, the Centre for Inflammation Research, Queen's Medical Research Institute, Edinburgh, United Kingdom
  • ,
  • William A. Wallace

      Affiliations

    • Department of Pathology, Royal Infirmary of Edinburgh, University of Edinburgh, Edinburgh, United Kingdom
    • Division of Pathology, College of Medicine and Veterinary Medicine, University of Edinburgh, Edinburgh, United Kingdom
  • ,
  • Kostas Kostarelos

      Affiliations

    • Nanomedicine Laboratory, Centre for Drug Delivery Research, the School of Pharmacy, University of London, London, United Kingdom
  • ,
  • Ken Donaldson

      Affiliations

    • University of Edinburgh/Medical Research Council, the Centre for Inflammation Research, Queen's Medical Research Institute, Edinburgh, United Kingdom
    • Corresponding Author InformationAddress reprint request to Ken Donaldson, Ph.D., Centre for Inflammation Research, Queen's Medical Research Institute, 47 Little France Crescent, Edinburgh EH16 4TJ, United Kingdom

Accepted 9 February 2011.

The fibrous shape of carbon nanotubes (CNTs) raises concern that they may pose an asbestos-like inhalation hazard, leading to the development of diseases, especially mesothelioma. Direct instillation of long and short CNTs into the pleural cavity, the site of mesothelioma development, produced asbestos-like length-dependent responses. The response to long CNTs and long asbestos was characterized by acute inflammation, leading to progressive fibrosis on the parietal pleura, where stomata of strictly defined size limit the egress of long, but not short, fibers. This was confirmed by demonstrating clearance of short, but not long, CNT and nickel nanowires and by visualizing the migration of short CNTs from the pleural space by single-photon emission computed tomographic imaging. Our data confirm the hypothesis that, although a proportion of all deposited particles passes through the pleura, the pathogenicity of long CNTs and other fibers arises as a result of length-dependent retention at the stomata on the parietal pleura.

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 Supported in part by the Department of Health (F.A.M.); The Colt Foundation (C.A.P. and K.D.); the EC FP7 NAMDIATREAM (NMP-2009-246479) research project (F.B. and A.P.-M.) and Science Foundation Ireland, as part of the CRANN CSET-funded facilities; and the European Commission FP7 ANTICARB (HEALTH-2008-20157) research project (K.T.A.-J., A.B., M.P., and K.K.).

 Author Contributions: F.A.M., C.A.P., R.D., and K.D. initiated, designed, and directed all experiments and took responsibility for planning and writing the manuscript; F.A.M., K.T.A.-J., A.N., and S.L. performed the SPECT/CT imaging experiment and analyzed the data; H.A.-B. performed transmission electron microscopy on the CNT panel; F.B., A.P.-M., and Y.V. manufactured and provided the NiNW samples and contributed to writing the manuscript; S.J.M. provided reagents and facilities for radiolabeling and SPECT/CT imaging; A.B., and M.P. prepared the short CNTs for labelling and analyzed the data; and S.L., A.B., W.M., and K.K. provided intellectual input and contributed to the writing of the manuscript.

 This is an independent report commissioned and funded by the Policy Research Programme in the Department of Health. The views expressed are not necessarily those of the Department.

PII: S0002-9440(11)00274-4

doi:10.1016/j.ajpath.2011.02.040

The American Journal of Pathology
Volume 178, Issue 6 , Pages 2587-2600, June 2011