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Is Occupational Asbestos Exposure an Under-Recognised Cause of Idiopathic Pulmonary Fibrosis?

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Is Occupational Asbestos Exposure an Under-Recognised Cause of Idiopathic Pulmonary Fibrosis? Is occupational asbestos exposure an under-recognised cause of idiopathic pulmonary fibrosis? Carl Jonathan Reynolds A thesis presented for the degree of Doctor of Philosophy Supervised by: Professor Paul Cullinan Dr Chris Barber Dr Sara De Matteis Department of Environmental and Occupational Medicine National Heart and Lung Institute Imperial College London, UK September 2020 Except where otherwise noted, content in this thesis is licensed under a Creative Commons Attribution 4.0 License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Copyright 2020, Carl Reynolds. 1 I, Carl Jonathan Reynolds confirm that the work presented in this thesis is my own. Where information has been derived from other sources, I confirm that this has been indicated in the thesis. 2 Abstract The question of whether occupational asbestos exposure is an under- recognized cause of idiopathic pulmonary fibrosis arises because it is clinically and epidemiologically plausible, and consistent with fibre studies, case-control, and toxicological data. This thesis examines the question by means of a literature review and a novel hospital based case-control study, the idiopathic pulmonary fibrosis job exposures study (IPFJES). In a literature review and meta-analysis of studies reporting on occupational exposures in idiopathic pulmonary fibrosis (IPF) I found significant associ- ations with metal, wood, and stone dust, but not asbestos. However, there was considerable heterogeneity and confidence in the meta-analysis result is tempered by a high risk of bias arising from selection, lack of blinding, exposure misclassification, incomplete exposure data, and selective report- ing of exposures. In a mortality analysis I found that the UK incidence of IPF continues to rise and appears to be correlated with mesothelioma mor- tality. I did not find clear evidence of an association between IPF, pleural mesothelioma, and asbestosis at a regional level. In a critical review of methods for assessing occupational asbestos exposure I found support for the use of a job exposure matrix based on proportional mortality rates for mesothelioma and validated by quantification of asbestos fibre lung burden. I also found support for using a structured interview tool to provide a quantitative estimate of previous exposure which was validated using historic and simulated exposure data. In a review of MUC5b and IPF I found evidence supporting a common MUC5b driven pulmonary fibrosis endotype and a candidate mechanism for 3 occupational asbestos exposure contributing to this; alveolar macrophage NLRP3 inflammasome activation resulting in increased IL-1β driven airway MUC5b expression. Occupational asbestos exposure alone was not associated with IPF in IPF- JES. It was associated with dyspnoea independent of smoking and case status. It was associated with IPF in participants who also had smoking exposure and the strength of this association was greatest for participants with the minor allele of the MUC5b promoter variant rs3505950 and when a stricter case definition (definite UIP rather than definite UIP or possible UIP) was used. These studies suggest that occupational asbestos exposure in smokers, cou- pled with genetic susceptibility factors, may be an important cause of IPF. 4 Acknowledgements I am particularly grateful to Paul Cullinan for his clear thinking, patience, kindness, and generous support. I am grateful to Paul Cullinan, Chris Barber, and Sara De Matteis for super- vising my thesis. I am grateful to Onn Min Kon for being my mentor. I am grateful to all of the IPFJES participants, the IPFJES team and collabora- tors including Athol Wells, Toby Maher, Tony Newman-Taylor, Paul Blanc, Kristin Cummings, Denis Vinnikov, John Cherrie, Rupa Sisodia, Caitlin Fitzgerald, Audrey Byrne, Cosetta Minelli, Miriam Moffatt, Magda Wheat- ley, Sophie Fletcher, Gareth Walters, Lisa Spenser, Helen Parfrey, Gauri Saini, Nazia Chaudhuri, Alex West, Huzaifa Adamali, Paul Beirne, Ian For- rest, Michael Gibbons, Justin Pepperell, Nik Hirani, Kim Harrison, Owen Dempsey, Steve O’Hickey, David Thickett, Dhruv Parekh, Suresh Babu, An- drew Wilson, George Chalmers, Melissa Wickremasinghe, and Robina Coker. I am grateful to Laura-Jayne Smith, Tom Yates, and Ehsan Ghorani for their friendship, support, and example. I am grateful to Alexandra Elbakyani, Li- nus Torvalds, Richard Stallman, Guido van Rossum, Wes McKinney, David Miller, Fred Kingham, and many other open source software developers and funders for providing and supporting the tools necessary to carry out my research. I am grateful to the Wellcome Trust (Wellcome Trust clinical research Training Fellowship grant 201291/Z/16/Z) and NIHR (CPMS ID 203355) for funding my work. I am thankful to Zeinab, Ada, and Rosa for putting up with me and giving me so much joy and happiness. To my Mum, Dad, and Sister for their love and support. 5 Table of Contents Abstract 3 Acknowledgements 5 List of figures 12 List of tables 13 Abbreviations 17 1 Introduction to thesis 18 1.1 Occupational asbestos exposure as an under-recognised cause of idiopathic pulmonary fibrosis . 18 1.2 Aims and objectives ..................... 19 1.3 Data sources ......................... 20 1.4 Outline of thesis ....................... 20 2 Literature review and meta-analysis: how much IPF is attributable to occupational exposures? 21 2.1 Introduction ......................... 21 2.2 Method ............................ 23 2.3 Results ............................ 24 2.3.1 Table 2.1: Previous IPF case-control studies reporting on occupational exposures. (Blanc 2019) . 24 2.3.2 Table 2.2: Overview of occupational IPF studies . 26 2.3.3 Table 2.3: Rob-SPEO risk of bias scores for occupa- tional IPF studies. 28 6 2.3.4 Table 2.4: Pooled population attributable risk fac- tors for occupation and idiopathic pulmonary fibrosis. (Blanc 2019) ..................... 29 2.4 Discussion .......................... 34 2.5 Conclusion .......................... 35 3 Mortality analysis: do mortality trends support an occu- pational cause? 37 3.1 Introduction ......................... 37 3.2 Method ............................ 38 3.3 Results ............................ 38 3.3.1 Table 3.1: Regional IPF, mesothelioma, and asbestosis mortality 1974-2012. Adjusted mortality rate ratios. 41 3.4 Discussion .......................... 41 3.5 Conclusion .......................... 44 4 Historic asbestos exposure assessment: can it be done? 45 4.1 Introduction ......................... 45 4.2 Method ............................ 46 4.3 Results ............................ 47 4.3.1 Lung biopsy and bronchoalveolar lavage . 47 4.3.2 Historic workplace measurements . 48 4.3.3 Exposure reconstruction . 49 4.3.3.1 Job-exposure matrices . 51 4.3.3.2 Exposure modelling approaches . 53 4.3.3.3 Self-reported exposure . 54 4.4 Discussion .......................... 55 4.5 Conclusion .......................... 56 5 MUC5b + environmental insult = IPF? 58 5.1 Introduction ......................... 58 5.1.1 Mucus, Mucins, MUC5b: structure, function and evo- lutionary importance . 58 5.1.2 MUC5b rs3570950 and respiratory disease . 61 5.1.3 Potential role of rs5270590 variant in IPF pathogenesis 62 5.1.4 Infection and immunity . 65 7 5.1.5 Inorganic occupational stimuli . 66 5.2 Conclusion .......................... 67 6 Idiopathic pulmonary fibrosis job exposures study (IPFJES): Is occupational asbestos exposure an under- recognised cause of IPF? 68 6.1 Introduction ......................... 68 6.2 Overview ........................... 69 6.3 Method ............................ 70 6.3.1 Funding, approvals, and registration . 70 6.3.2 Selection ....................... 70 6.3.3 Measures ....................... 72 6.3.4 Statistical analysis . 74 6.4 Results ............................ 75 6.4.1 Table 6.1: Participant demographic characteristics . 77 6.4.2 Table 6.2: Patient clinical features (from case report form) and genotypes . 78 6.4.3 Table 6.3: Centre control clinics and recruitment . 81 6.4.4 Table 6.4: Radiological findings and occupational as- bestos exposure (inferred by job title) by centre (N=960) 82 6.4.5 Table 6.5: Occupational asbestos exposure (inferred by job title) and IPF risk (ever vs never) . 83 6.4.6 Table 6.6: Occupational asbestos exposure (inferred by job title) and IPF risk (categories of exposure) . 84 6.4.7 Table 6.7: Source receptor model parameter summary statistics ....................... 87 6.4.8 Illustrative example source receptor model assessment based on a real case . 87 6.4.9 Table 6.8: Occupational asbestos exposure (cumula- tive fibre ml year estimate) and IPF risk . 89 6.4.10 Table 6.9: MUC5b rs35705950, occupational asbestos exposure, smoking, and IPF risk . 91 6.4.11 Table 6.10: MUC5b rs35705950, occupational asbestos exposure, smoking, and IPF risk (definite UIP only) . 92 8 6.4.12 Table 6.11: Unadjusted and adjusted OR for IPF risk factors potential confounders . 94 6.4.13 Table 6.12: Occupational metal, wood, and stone ex- posure and IPF risk . 95 6.4.14 Table 6.13: Sensitivity analysis (limited to jobs that ended before 1980): Occupational asbestos exposure (inferred by job title) and IPF risk (ever vs never) N=779 96 6.4.15 Table 6.14: Sensitivity analysis (limited to jobs that ended before 1980): Occupational asbestos exposure (inferred by job title) and IPF risk (categories of expo- sure) N=779 ..................... 96 6.4.16 Table 6.15: Sensitivity analysis
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