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Open Access
Peer-reviewed
Research Article
Particulate Matter from Both Heavy Fuel Oil and Diesel Fuel Shipping Emissions Show Strong Biological Effects on Human Lung Cells at Realistic and Comparable In Vitro Exposure Conditions
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Sebastian Oeder ,
Contributed equally to this work with: Sebastian Oeder, Tamara Kanashova, Olli Sippula, Sean C. Sapcariu, Thorsten Streibel, Jose Manuel Arteaga-Salas, Johannes Passig
Affiliations HICE—Helmholtz Virtual Institute of Complex Molecular Systems in Environmental Health—Aerosols and Health, www.hice-vi.eu, Neuherberg, Rostock, Munich, Karlsruhe, Berlin, Waldkirch, Germany, Kuopio, Finland, Cardiff, UK, Esch-Belval, Luxembourg, Center of Allergy and Environment (ZAUM), Helmholtz Zentrum München and Technische Universität München, Member of the German Center for Lung Research (DZL), Munich, Germany, CK-CARE, Christine Kühne Center for Allergy Research and Education, Davos, Switzerland
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Tamara Kanashova ,
Contributed equally to this work with: Sebastian Oeder, Tamara Kanashova, Olli Sippula, Sean C. Sapcariu, Thorsten Streibel, Jose Manuel Arteaga-Salas, Johannes Passig
Affiliations HICE—Helmholtz Virtual Institute of Complex Molecular Systems in Environmental Health—Aerosols and Health, www.hice-vi.eu, Neuherberg, Rostock, Munich, Karlsruhe, Berlin, Waldkirch, Germany, Kuopio, Finland, Cardiff, UK, Esch-Belval, Luxembourg, Mass Spectrometry Core Unit, Max Delbrück Center for Molecular Medicine Berlin-Buch, Germany
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Olli Sippula ,
Contributed equally to this work with: Sebastian Oeder, Tamara Kanashova, Olli Sippula, Sean C. Sapcariu, Thorsten Streibel, Jose Manuel Arteaga-Salas, Johannes Passig
Affiliations HICE—Helmholtz Virtual Institute of Complex Molecular Systems in Environmental Health—Aerosols and Health, www.hice-vi.eu, Neuherberg, Rostock, Munich, Karlsruhe, Berlin, Waldkirch, Germany, Kuopio, Finland, Cardiff, UK, Esch-Belval, Luxembourg, University of Eastern Finland, Department of Environmental Science, P.O. Box 1627, FI-70211 Kuopio, Finland
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Sean C. Sapcariu ,
Contributed equally to this work with: Sebastian Oeder, Tamara Kanashova, Olli Sippula, Sean C. Sapcariu, Thorsten Streibel, Jose Manuel Arteaga-Salas, Johannes Passig
Affiliations HICE—Helmholtz Virtual Institute of Complex Molecular Systems in Environmental Health—Aerosols and Health, www.hice-vi.eu, Neuherberg, Rostock, Munich, Karlsruhe, Berlin, Waldkirch, Germany, Kuopio, Finland, Cardiff, UK, Esch-Belval, Luxembourg, Luxembourg Centre for Systems Biomedicine, University of Luxembourg, L-4362 Esch-Belval, Luxembourg
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Thorsten Streibel ,
Contributed equally to this work with: Sebastian Oeder, Tamara Kanashova, Olli Sippula, Sean C. Sapcariu, Thorsten Streibel, Jose Manuel Arteaga-Salas, Johannes Passig
Affiliations HICE—Helmholtz Virtual Institute of Complex Molecular Systems in Environmental Health—Aerosols and Health, www.hice-vi.eu, Neuherberg, Rostock, Munich, Karlsruhe, Berlin, Waldkirch, Germany, Kuopio, Finland, Cardiff, UK, Esch-Belval, Luxembourg, Joint Mass Spectrometry Centre, Chair of Analytical Chemistry, Institute of Chemistry, University Rostock, Rostock, Germany, Joint Mass Spectrometry Centre, CMA—Comprehensive Molecular Analytics, Helmholtz Zentrum München, Neuherberg, Germany
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Jose Manuel Arteaga-Salas ,
Contributed equally to this work with: Sebastian Oeder, Tamara Kanashova, Olli Sippula, Sean C. Sapcariu, Thorsten Streibel, Jose Manuel Arteaga-Salas, Johannes Passig
Affiliations HICE—Helmholtz Virtual Institute of Complex Molecular Systems in Environmental Health—Aerosols and Health, www.hice-vi.eu, Neuherberg, Rostock, Munich, Karlsruhe, Berlin, Waldkirch, Germany, Kuopio, Finland, Cardiff, UK, Esch-Belval, Luxembourg, Joint Mass Spectrometry Centre, CMA—Comprehensive Molecular Analytics, Helmholtz Zentrum München, Neuherberg, Germany
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Johannes Passig ,
Contributed equally to this work with: Sebastian Oeder, Tamara Kanashova, Olli Sippula, Sean C. Sapcariu, Thorsten Streibel, Jose Manuel Arteaga-Salas, Johannes Passig
Affiliations HICE—Helmholtz Virtual Institute of Complex Molecular Systems in Environmental Health—Aerosols and Health, www.hice-vi.eu, Neuherberg, Rostock, Munich, Karlsruhe, Berlin, Waldkirch, Germany, Kuopio, Finland, Cardiff, UK, Esch-Belval, Luxembourg, Joint Mass Spectrometry Centre, Chair of Analytical Chemistry, Institute of Chemistry, University Rostock, Rostock, Germany
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Marco Dilger,
Affiliations HICE—Helmholtz Virtual Institute of Complex Molecular Systems in Environmental Health—Aerosols and Health, www.hice-vi.eu, Neuherberg, Rostock, Munich, Karlsruhe, Berlin, Waldkirch, Germany, Kuopio, Finland, Cardiff, UK, Esch-Belval, Luxembourg, Institute for Technical Chemistry (ITC), Karlsruhe Institute of Technology, Campus North, Karlsruhe, Germany, Institute of Toxicology and Genetics (ITG), Karlsruhe Institute of Technology, Campus North, Karlsruhe, Germany
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Hanns-Rudolf Paur,
Affiliations HICE—Helmholtz Virtual Institute of Complex Molecular Systems in Environmental Health—Aerosols and Health, www.hice-vi.eu, Neuherberg, Rostock, Munich, Karlsruhe, Berlin, Waldkirch, Germany, Kuopio, Finland, Cardiff, UK, Esch-Belval, Luxembourg, Institute for Technical Chemistry (ITC), Karlsruhe Institute of Technology, Campus North, Karlsruhe, Germany
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Christoph Schlager,
Affiliations HICE—Helmholtz Virtual Institute of Complex Molecular Systems in Environmental Health—Aerosols and Health, www.hice-vi.eu, Neuherberg, Rostock, Munich, Karlsruhe, Berlin, Waldkirch, Germany, Kuopio, Finland, Cardiff, UK, Esch-Belval, Luxembourg, Institute for Technical Chemistry (ITC), Karlsruhe Institute of Technology, Campus North, Karlsruhe, Germany
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Sonja Mülhopt,
Affiliations HICE—Helmholtz Virtual Institute of Complex Molecular Systems in Environmental Health—Aerosols and Health, www.hice-vi.eu, Neuherberg, Rostock, Munich, Karlsruhe, Berlin, Waldkirch, Germany, Kuopio, Finland, Cardiff, UK, Esch-Belval, Luxembourg, Institute for Technical Chemistry (ITC), Karlsruhe Institute of Technology, Campus North, Karlsruhe, Germany
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Silvia Diabaté,
Affiliations HICE—Helmholtz Virtual Institute of Complex Molecular Systems in Environmental Health—Aerosols and Health, www.hice-vi.eu, Neuherberg, Rostock, Munich, Karlsruhe, Berlin, Waldkirch, Germany, Kuopio, Finland, Cardiff, UK, Esch-Belval, Luxembourg, Institute of Toxicology and Genetics (ITG), Karlsruhe Institute of Technology, Campus North, Karlsruhe, Germany
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Carsten Weiss,
Affiliations HICE—Helmholtz Virtual Institute of Complex Molecular Systems in Environmental Health—Aerosols and Health, www.hice-vi.eu, Neuherberg, Rostock, Munich, Karlsruhe, Berlin, Waldkirch, Germany, Kuopio, Finland, Cardiff, UK, Esch-Belval, Luxembourg, Institute of Toxicology and Genetics (ITG), Karlsruhe Institute of Technology, Campus North, Karlsruhe, Germany
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Benjamin Stengel,
Affiliations HICE—Helmholtz Virtual Institute of Complex Molecular Systems in Environmental Health—Aerosols and Health, www.hice-vi.eu, Neuherberg, Rostock, Munich, Karlsruhe, Berlin, Waldkirch, Germany, Kuopio, Finland, Cardiff, UK, Esch-Belval, Luxembourg, Chair of Piston Machines and Internal Combustion Engines, University Rostock, Rostock, Germany
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Rom Rabe,
Affiliations HICE—Helmholtz Virtual Institute of Complex Molecular Systems in Environmental Health—Aerosols and Health, www.hice-vi.eu, Neuherberg, Rostock, Munich, Karlsruhe, Berlin, Waldkirch, Germany, Kuopio, Finland, Cardiff, UK, Esch-Belval, Luxembourg, Chair of Piston Machines and Internal Combustion Engines, University Rostock, Rostock, Germany
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Horst Harndorf,
Affiliations HICE—Helmholtz Virtual Institute of Complex Molecular Systems in Environmental Health—Aerosols and Health, www.hice-vi.eu, Neuherberg, Rostock, Munich, Karlsruhe, Berlin, Waldkirch, Germany, Kuopio, Finland, Cardiff, UK, Esch-Belval, Luxembourg, Chair of Piston Machines and Internal Combustion Engines, University Rostock, Rostock, Germany
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Tiina Torvela,
Affiliation University of Eastern Finland, Department of Environmental Science, P.O. Box 1627, FI-70211 Kuopio, Finland
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Jorma K. Jokiniemi,
Affiliations HICE—Helmholtz Virtual Institute of Complex Molecular Systems in Environmental Health—Aerosols and Health, www.hice-vi.eu, Neuherberg, Rostock, Munich, Karlsruhe, Berlin, Waldkirch, Germany, Kuopio, Finland, Cardiff, UK, Esch-Belval, Luxembourg, University of Eastern Finland, Department of Environmental Science, P.O. Box 1627, FI-70211 Kuopio, Finland, VTT Technical Research Centre of Finland, P.O. Box 1000, FI-02044 VTT, Espoo, Finland
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Maija-Riitta Hirvonen,
Affiliations HICE—Helmholtz Virtual Institute of Complex Molecular Systems in Environmental Health—Aerosols and Health, www.hice-vi.eu, Neuherberg, Rostock, Munich, Karlsruhe, Berlin, Waldkirch, Germany, Kuopio, Finland, Cardiff, UK, Esch-Belval, Luxembourg, University of Eastern Finland, Department of Environmental Science, P.O. Box 1627, FI-70211 Kuopio, Finland, National Institute for Health and Welfare, Department of Environmental Health, P.O. Box 95, FI-70701, Kuopio, Finland
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Carsten Schmidt-Weber,
Affiliation Center of Allergy and Environment (ZAUM), Helmholtz Zentrum München and Technische Universität München, Member of the German Center for Lung Research (DZL), Munich, Germany
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Claudia Traidl-Hoffmann,
Affiliations CK-CARE, Christine Kühne Center for Allergy Research and Education, Davos, Switzerland, Institute of environmental medicine, UNIKA-T, Technische Universität, Munich, Germany
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Kelly A. BéruBé,
Affiliations HICE—Helmholtz Virtual Institute of Complex Molecular Systems in Environmental Health—Aerosols and Health, www.hice-vi.eu, Neuherberg, Rostock, Munich, Karlsruhe, Berlin, Waldkirch, Germany, Kuopio, Finland, Cardiff, UK, Esch-Belval, Luxembourg, Lung and Particle Research Group, School of Biosciences, Cardiff University, Cardiff, Wales, United Kingdom
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Anna J. Wlodarczyk,
Affiliations HICE—Helmholtz Virtual Institute of Complex Molecular Systems in Environmental Health—Aerosols and Health, www.hice-vi.eu, Neuherberg, Rostock, Munich, Karlsruhe, Berlin, Waldkirch, Germany, Kuopio, Finland, Cardiff, UK, Esch-Belval, Luxembourg, Lung and Particle Research Group, School of Biosciences, Cardiff University, Cardiff, Wales, United Kingdom
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Zoë Prytherch,
Affiliations HICE—Helmholtz Virtual Institute of Complex Molecular Systems in Environmental Health—Aerosols and Health, www.hice-vi.eu, Neuherberg, Rostock, Munich, Karlsruhe, Berlin, Waldkirch, Germany, Kuopio, Finland, Cardiff, UK, Esch-Belval, Luxembourg, Lung and Particle Research Group, School of Biosciences, Cardiff University, Cardiff, Wales, United Kingdom
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Bernhard Michalke,
Affiliation Research Unit Analytical BioGeoChemistry, Helmholtz Zentrum München—German Research Center for Environmental Health GmbH, Neuherberg, Germany
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Tobias Krebs,
Affiliations HICE—Helmholtz Virtual Institute of Complex Molecular Systems in Environmental Health—Aerosols and Health, www.hice-vi.eu, Neuherberg, Rostock, Munich, Karlsruhe, Berlin, Waldkirch, Germany, Kuopio, Finland, Cardiff, UK, Esch-Belval, Luxembourg, Vitrocell GmbH, Waldkirch, Germany
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André S. H. Prévôt,
Affiliation Laboratory of Atmospheric Chemistry, Paul Scherrer Institute (PSI), Villigen, Switzerland
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Michael Kelbg,
Affiliations HICE—Helmholtz Virtual Institute of Complex Molecular Systems in Environmental Health—Aerosols and Health, www.hice-vi.eu, Neuherberg, Rostock, Munich, Karlsruhe, Berlin, Waldkirch, Germany, Kuopio, Finland, Cardiff, UK, Esch-Belval, Luxembourg, Institute of Physics, University Rostock, Rostock, Germany
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Josef Tiggesbäumker,
Affiliations HICE—Helmholtz Virtual Institute of Complex Molecular Systems in Environmental Health—Aerosols and Health, www.hice-vi.eu, Neuherberg, Rostock, Munich, Karlsruhe, Berlin, Waldkirch, Germany, Kuopio, Finland, Cardiff, UK, Esch-Belval, Luxembourg, Institute of Physics, University Rostock, Rostock, Germany
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Erwin Karg,
Affiliation Joint Mass Spectrometry Centre, CMA—Comprehensive Molecular Analytics, Helmholtz Zentrum München, Neuherberg, Germany
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Gert Jakobi,
Affiliation Joint Mass Spectrometry Centre, CMA—Comprehensive Molecular Analytics, Helmholtz Zentrum München, Neuherberg, Germany
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Sorana Scholtes,
Affiliations HICE—Helmholtz Virtual Institute of Complex Molecular Systems in Environmental Health—Aerosols and Health, www.hice-vi.eu, Neuherberg, Rostock, Munich, Karlsruhe, Berlin, Waldkirch, Germany, Kuopio, Finland, Cardiff, UK, Esch-Belval, Luxembourg, Joint Mass Spectrometry Centre, CMA—Comprehensive Molecular Analytics, Helmholtz Zentrum München, Neuherberg, Germany
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Jürgen Schnelle-Kreis,
Affiliation Joint Mass Spectrometry Centre, CMA—Comprehensive Molecular Analytics, Helmholtz Zentrum München, Neuherberg, Germany
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Jutta Lintelmann,
Affiliation Joint Mass Spectrometry Centre, CMA—Comprehensive Molecular Analytics, Helmholtz Zentrum München, Neuherberg, Germany
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Georg Matuschek,
Affiliation Joint Mass Spectrometry Centre, CMA—Comprehensive Molecular Analytics, Helmholtz Zentrum München, Neuherberg, Germany
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Martin Sklorz,
Affiliation Joint Mass Spectrometry Centre, Chair of Analytical Chemistry, Institute of Chemistry, University Rostock, Rostock, Germany
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Sophie Klingbeil,
Affiliations HICE—Helmholtz Virtual Institute of Complex Molecular Systems in Environmental Health—Aerosols and Health, www.hice-vi.eu, Neuherberg, Rostock, Munich, Karlsruhe, Berlin, Waldkirch, Germany, Kuopio, Finland, Cardiff, UK, Esch-Belval, Luxembourg, Joint Mass Spectrometry Centre, Chair of Analytical Chemistry, Institute of Chemistry, University Rostock, Rostock, Germany
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Jürgen Orasche,
Affiliation Joint Mass Spectrometry Centre, CMA—Comprehensive Molecular Analytics, Helmholtz Zentrum München, Neuherberg, Germany
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Patrick Richthammer,
Affiliations HICE—Helmholtz Virtual Institute of Complex Molecular Systems in Environmental Health—Aerosols and Health, www.hice-vi.eu, Neuherberg, Rostock, Munich, Karlsruhe, Berlin, Waldkirch, Germany, Kuopio, Finland, Cardiff, UK, Esch-Belval, Luxembourg, Joint Mass Spectrometry Centre, CMA—Comprehensive Molecular Analytics, Helmholtz Zentrum München, Neuherberg, Germany
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Laarnie Müller,
Affiliation Joint Mass Spectrometry Centre, CMA—Comprehensive Molecular Analytics, Helmholtz Zentrum München, Neuherberg, Germany
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Michael Elsasser,
Affiliation Joint Mass Spectrometry Centre, CMA—Comprehensive Molecular Analytics, Helmholtz Zentrum München, Neuherberg, Germany
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Ahmed Reda,
Affiliation Joint Mass Spectrometry Centre, CMA—Comprehensive Molecular Analytics, Helmholtz Zentrum München, Neuherberg, Germany
⨯ -
Thomas Gröger,
Affiliation Joint Mass Spectrometry Centre, CMA—Comprehensive Molecular Analytics, Helmholtz Zentrum München, Neuherberg, Germany
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Benedikt Weggler,
Affiliations HICE—Helmholtz Virtual Institute of Complex Molecular Systems in Environmental Health—Aerosols and Health, www.hice-vi.eu, Neuherberg, Rostock, Munich, Karlsruhe, Berlin, Waldkirch, Germany, Kuopio, Finland, Cardiff, UK, Esch-Belval, Luxembourg, Joint Mass Spectrometry Centre, CMA—Comprehensive Molecular Analytics, Helmholtz Zentrum München, Neuherberg, Germany
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Theo Schwemer,
Affiliation Joint Mass Spectrometry Centre, Chair of Analytical Chemistry, Institute of Chemistry, University Rostock, Rostock, Germany
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Hendryk Czech,
Affiliation Joint Mass Spectrometry Centre, Chair of Analytical Chemistry, Institute of Chemistry, University Rostock, Rostock, Germany
⨯ -
Christopher P. Rüger,
Affiliation Joint Mass Spectrometry Centre, Chair of Analytical Chemistry, Institute of Chemistry, University Rostock, Rostock, Germany
⨯ -
Gülcin Abbaszade,
Affiliation Joint Mass Spectrometry Centre, CMA—Comprehensive Molecular Analytics, Helmholtz Zentrum München, Neuherberg, Germany
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Christian Radischat,
Affiliations HICE—Helmholtz Virtual Institute of Complex Molecular Systems in Environmental Health—Aerosols and Health, www.hice-vi.eu, Neuherberg, Rostock, Munich, Karlsruhe, Berlin, Waldkirch, Germany, Kuopio, Finland, Cardiff, UK, Esch-Belval, Luxembourg, Joint Mass Spectrometry Centre, Chair of Analytical Chemistry, Institute of Chemistry, University Rostock, Rostock, Germany
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Karsten Hiller,
Affiliations HICE—Helmholtz Virtual Institute of Complex Molecular Systems in Environmental Health—Aerosols and Health, www.hice-vi.eu, Neuherberg, Rostock, Munich, Karlsruhe, Berlin, Waldkirch, Germany, Kuopio, Finland, Cardiff, UK, Esch-Belval, Luxembourg, Luxembourg Centre for Systems Biomedicine, University of Luxembourg, L-4362 Esch-Belval, Luxembourg
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Jeroen T. M. Buters ,
¶‡ These authors also contributed equally to the manuscript.
Affiliations HICE—Helmholtz Virtual Institute of Complex Molecular Systems in Environmental Health—Aerosols and Health, www.hice-vi.eu, Neuherberg, Rostock, Munich, Karlsruhe, Berlin, Waldkirch, Germany, Kuopio, Finland, Cardiff, UK, Esch-Belval, Luxembourg, Center of Allergy and Environment (ZAUM), Helmholtz Zentrum München and Technische Universität München, Member of the German Center for Lung Research (DZL), Munich, Germany, CK-CARE, Christine Kühne Center for Allergy Research and Education, Davos, Switzerland
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Gunnar Dittmar ,
¶‡ These authors also contributed equally to the manuscript.
Affiliations HICE—Helmholtz Virtual Institute of Complex Molecular Systems in Environmental Health—Aerosols and Health, www.hice-vi.eu, Neuherberg, Rostock, Munich, Karlsruhe, Berlin, Waldkirch, Germany, Kuopio, Finland, Cardiff, UK, Esch-Belval, Luxembourg, Mass Spectrometry Core Unit, Max Delbrück Center for Molecular Medicine Berlin-Buch, Germany
⨯ - [ ... ],
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Ralf Zimmermann
* E-mail: ralf.zimmermann@helmholtz-muenchen.de
¶‡ These authors also contributed equally to the manuscript.
Affiliations HICE—Helmholtz Virtual Institute of Complex Molecular Systems in Environmental Health—Aerosols and Health, www.hice-vi.eu, Neuherberg, Rostock, Munich, Karlsruhe, Berlin, Waldkirch, Germany, Kuopio, Finland, Cardiff, UK, Esch-Belval, Luxembourg, Joint Mass Spectrometry Centre, Chair of Analytical Chemistry, Institute of Chemistry, University Rostock, Rostock, Germany, Joint Mass Spectrometry Centre, CMA—Comprehensive Molecular Analytics, Helmholtz Zentrum München, Neuherberg, Germany
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Particulate Matter from Both Heavy Fuel Oil and Diesel Fuel Shipping Emissions Show Strong Biological Effects on Human Lung Cells at Realistic and Comparable In Vitro Exposure Conditions
- Sebastian Oeder,
- Tamara Kanashova,
- Olli Sippula,
- Sean C. Sapcariu,
- Thorsten Streibel,
- Jose Manuel Arteaga-Salas,
- Johannes Passig,
- Marco Dilger,
- Hanns-Rudolf Paur,
- Christoph Schlager

- Published: June 3, 2015
- https://doi.org/10.1371/journal.pone.0126536