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Editorial

Diesel engine exhaust classified as a human lung carcinogen. How will this affect occupational exposures? Paul T J Scheepers,1 Roel C H Vermeulen2 A Working Group of the International Agency for Research on Cancer (IARC) convened in Lyon, France, June 5–12 to scrutinise the available knowledge base on the carcinogenicity of diesel engine exhaust, gasoline engine exhaust and some nitroarenes.1 Diesel and gasoline engine exhaust and nitroarenes were previously evaluated by IARC in 1989.2 For gasoline engine exhaust the classification remained Group 2B (‘possibly carcinogenic to humans’) as well as for seven of the nitroarenes. The newly evaluated nitroarene 3-nitrobenzanthrone was also added to this group. 6-Nitrochrysene and 1-nitropyrene were classified as 2A ‘Probably carcinogenic to humans’. 6-Nitrochrysene and 1-nitropyrene are important exposure markers for diesel exhaust since metabolites of these substances have been found in workers exposed to diesel exhaust.3–5 The most prominent outcome of the IARC evaluation meeting was the upgrade of the classification of diesel exhaust, now in Group 1 ‘Carcinogenic to humans’ with sufficient evidence for lung cancer and limited evidence for bladder cancer. For diesel engine exhaust the change from Group 2A to Group 1 was primarily driven by new evidence from epidemiological studies in the mining and trucking industry. The most recent study performed in underground ‘non-metal mining’ included 12 315 miners from salt (sodium chloride), potash ( potassium carbonate), trona (sodium carbonate), and limestone mines.6 7 Miners were exposed to relative high diesel exhaust exposure 1 Department of Epidemiology Biostatistics and HTA (133), Radboud University Nijmegen Medical Centre, Nijmegen, The Netherlands 2 Institute of Risk Assessment Sciences, University of Utrecht, The Netherlands

Correspondence to Dr Paul T J Scheepers, Department of Epidemiology Biostatistics and HTA (133), Radboud University Nijmegen Medical Centre, PO Box 9101, 6500HB Nijmegen, The Netherlands; [email protected]

Occup Environ Med October 2012 Vol 69 No 10

levels and had no or very low co-exposures to asbestos, silica, uranium and radon. Average intensity of respirable elemental carbon (REC) exposure, based on each individual’s full work history at the study facilities, was 87.0 μg/m3 for all workers, 128.2 μg/m3 for ever-underground workers, and 1.7 μg/m3 for surfaceonly workers.6 In the trucking study the exposure of 31 135 truck drivers to diesel engine exhaust was estimated based on measurements of REC in 1988–1989 and 2001–2006 in this industry.8 Average intensity of REC exposure, in this study was around 4 μg/m3 9. Both the mining and trucking studies showed a clear dose–response relationship between exposure to diesel engine exhaust as estimated by REC and lung cancer risk. In addition to these large cohort studies, a number of smaller occupational studies and several case–control studies in the general population also generally indicated an increased level of lung cancer related to exposure to diesel engine exhaust. The classification of diesel engine exhaust as a Group 1 carcinogen is not only based on evidence from human data. The relationship with cancer was also supported by experimental studies in animals and information on working mechanisms from in vitro studies. Since the previous evaluation in 1989, several studies in rats have been conducted that showed an inflammatory response to inhalation of diesel engine exhaust. A similar response has, however, been observed for other types of particles, largely devoid of genotoxic substances, like carbon black and titanium dioxide. In these rat studies, lung tumours were only induced at extremely high doses. The IARC Working Group adopted the inflammatory mechanism, involvement of cytokines and reactive oxygen species, as an important determinant of the formation of tumours relevant for the cancer risk in humans. The Working

Group also noted that the specific sensitivity of rats to ‘overload’ conditions is well understood but that the study results are of limited relevance for the interpretation of the lung cancer risk in (low dose) human situations. The Working Group acknowledged the overwhelming and convincing evidence for a genotoxic working mechanisms, based on in vitro studies of diesel engine particles and their organic extracts. The observed responses in these studies are explained by the presence of genotoxic species like polycyclic aromatic hydrocarbons (PAHs) and nitroarenes. Mutations have been observed that are involved in initiation, promotion and progression stages of tumour formation. For these substances the mechanism of tumour formation is sufficiently clear to support strong mechanistic evidence for the carcinogenicity of diesel engine exhaust. Diesel engines have progressed from traditional technology (2007/standards Euro 6/US2010), characterised by the integration of wall-flow diesel particulate filter and diesel oxidation catalyst. The major compositional changes in diesel exhaust by the new technology are the virtual elimination of the elemental carbon core, reduced semi-volatile fraction, lower concentrations of PAHs, lower sulphates and lower particle number emissions. On a per-km or per-kw-h basis, particulate mass is reduced by over 99% and NOx by 98% compared to traditional engines. An interesting consequence of the introduction of new technology engines is that elemental carbon will be virtually eliminated. However, the genotoxic organic compounds may still be present, although at much lower levels. The consequence of this might be that these genotoxic compounds will no longer be adsorbed to carbon cores. Since many of the low volatile compounds will not remain in the gas phase they will either become part of an organic condensate in the nucleation mode or adsorb to other solids in the engine exhaust such as metal oxides or sulphate particles. In either case they will appear in the workplace atmospheres as ultrafine particles which may alter their lung uptake and bioavailability, compared to the emission from traditional and transitional engine technologies. 691

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Editorial

Figure 1 Implementation schedule of global on-highway heavy diesel duty diesel engine emission standards. Grey boxes: No particulate matter standards ‘Traditional engines’. The shaded area with diagonal lines indicates the introduction of new technology diesel engines. Period in between delineates transitional engine technology with increasingly more stringent emission standards (Euro 1/US 1988 to Euro 6/US2010). For workplaces, substitution of traditional and transitional engine technology by ‘new technology’ engines will probably result in lower emissions. This is likely a better option than retrofitting of soot

filters and oxidation catalysers on the tailpipe of old engines, which may sometimes lead to an increase of toxic compounds in the gas phase (aldehydes) or in the particle phase (nitroarenes).10

The rate of conversion of older to newer technology will be largely driven by US and European regulation with other countries generally following several years later (see figures 1 and 2). Furthermore, the

Figure 2 Implementation schedule of global nonroad heavy diesel duty diesel engine emission standards. Grey boxes: No particulate matter standards ‘Traditional engines’. The shaded area with diagonal lines indicates the introduction of new technology diesel engines. Period in between delineates transitional engine technology with increasingly more stringent emission standards (Tier 2 to Tier 4). 692

Occup Environ Med October 2012 Vol 69 No 10

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Editorial conversion to new diesel technology will be quicker for on-highway vehicles than for non-road vehicles where regulation is currently less stringent. However, as newer engine technology will find its way into the fleet, most workers and the population at large will remain for many years, especially in less developed regions in the world, to be exposed to ‘traffic emissions’ from a mixture of new and old technology diesel engines. The recent classification of diesel engine exhaust as a human carcinogen calls for implementation of controls that reduce exposures at workplaces, specifically if engines are used in confined spaces. Replacement of traditional or transitional technology engines by new technology engines is preferred but will probably take decades. With this gradual introduction of low-emission engines, elemental carbon concentrations will likely decrease below current detection capabilities. This anticipated development may require alternative/additional proxies for future exposure assessment of diesel engine exhaust.

Occup Environ Med October 2012 Vol 69 No 10

Acknowledgements We would like to thank Dr John C Wall, Cummins Inc. for supplying the figures on emission standards. Contributors RL, PS were member of the International Agency for Research on Cancer Working Group and have contributed in conveying and writing the editorial.

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Competing interests None. Provenance and peer review Commissioned; internally peer reviewed.

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Accepted 21 August 2012 Occup Environ Med 2012;69:691–693. doi:10.1136/oemed-2012-101088

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Benbrahim-Tallaa L, Baan RA, Grosse Y, et al. Carcinogenicity of diesel-engine and gasoline-engine exhausts and some nitroarenes. Lancet Oncol 2012;13:663–4. IARC. IARC Monographs on the evaluation of carcinogenic risks to humans. Diesel and gasoline engine exhausts and some nitroarenes. International Agency for Research on Cancer. IARC Monogr Eval Carcinog Risks Hum. 1989;46:1–458. Scheepers PTJ, Thuis HJTM, Martens MHJ, et al. Assessment of occupational exposure to diesel exhaust. The use of an immunoassay for the determination of urinary metabolites of nitroarenes and polycyclic aromatic hydrocarbons. Toxicol Lett 1994;72:191–8.

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Zwirner-Baier I, Neumann HG. Polycyclic nitroarenes (nitro-PAHs) as biomarkers of exposure to diesel exhaust. Mutat Res 1999;441:135–44. Seidel A, Dahmann D, Krekeler H, et al. Biomonitoring of polycyclic aromatic compounds in the urine of mining workers occupationally exposed to diesel exhaust. Int J Hyg Environ Health 2002;204:333–8. Attfield MT, Schleiff PL, Lubin JH, et al. The diesel exhaust in miners study: a cohort mortality study with emphasis on lung cancer. J Natl Cancer Inst 2012;104:869–83. Silverman DT, Samanic CM, Lubin JH, et al. The diesel exhaust in miners study: a nested case–control study of lung cancer and diesel exhaust. J Natl Cancer Inst 2012;6:855–68. Davis ME, Hart JE, Laden F, et al. A retrospective assessment of occupational exposure to elemental carbon in the US trucking industry. Environ Health Perspect 2011;119:997–1002. Garshick E, Laden F, Hart JE, et al. Lung cancer and elemental carbon exposure in trucking industry workers. Environ Health Perspect. Published Online First: 1 June 2012. doi:10.1289/ehp. 1204989 Sharp CA, Howell SA, Jobe J. The effect of biodiesel fuels on transient emissions from modern diesel engines, Part II Unregulated emissions and chemical characterization. SAE Technical Paper Series, 2000-01-1968, 24 pp.

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Downloaded from oem.bmj.com on September 10, 2012 - Published by group.bmj.com

Diesel engine exhaust classified as a human lung carcinogen. How will this affect occupational exposures? Paul T J Scheepers and Roel C H Vermeulen Occup Environ Med 2012 69: 691-693

doi: 10.1136/oemed-2012-101088

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