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Published in: Respiratory Research 1/2021

Open Access 01-12-2021 | Idiopathic Pulmonary Fibrosis | Research

Exposure to PM2.5 is a risk factor for acute exacerbation of surgically diagnosed idiopathic pulmonary fibrosis: a case–control study

Authors: Masahiro Tahara, Yoshihisa Fujino, Kei Yamasaki, Keishi Oda, Takashi Kido, Noriho Sakamoto, Toshinori Kawanami, Kensuke Kataoka, Ryoko Egashira, Mikiko Hashisako, Yuzo Suzuki, Tomoyuki Fujisawa, Hiroshi Mukae, Takafumi Suda, Kazuhiro Yatera

Published in: Respiratory Research | Issue 1/2021

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Abstract

Background

Short-term exposure to ozone and nitrogen dioxide is a risk factor for acute exacerbation (AE) of idiopathic pulmonary fibrosis (AE-IPF). The comprehensive roles of exposure to fine particulate matter in AE-IPF remain unclear. We aim to investigate the association of short-term exposure to fine particulate matter with the incidence of AE-IPF and to determine the exposure-risk time window during 3 months before the diagnosis of AE-IPF.

Methods

IPF patients were retrospectively identified from the nationwide registry in Japan. We conducted a case–control study to assess the correlation between AE-IPF incidence and short-term exposure to eight air pollutants, including particulate matter < 2.5 µm (PM2.5). In the time-series data, we compared monthly mean exposure concentrations between months with AE (case months) and those without AE (control months). We used multilevel mixed-effects logistic regression models to consider individual and institutional-level variables, and also adjusted these models for several covariates, including temperature and humidity. An additional analysis with different monthly lag periods was conducted to determine the risk-exposure time window for 3 months before the diagnosis of AE-IPF.

Results

Overall, 152 patients with surgically diagnosed IPF were analyzed. AE-IPF was significantly associated with an increased mean exposure level of nitric oxide (NO) and PM2.5 30 days prior to AE diagnosis. Adjusted odds ratio (OR) with a 10 unit increase in NO was 1.46 [95% confidence interval (CI) 1.11–1.93], and PM2.5 was 2.56 (95% CI 1.27–5.15). Additional analysis revealed that AE-IPF was associated with exposure to NO during the lag periods lag 1, lag 2, lag 1–2, and lag 1–3, and PM2.5 during the lag periods lag 1 and lag 1–2.

Conclusions

Our results show that PM2.5 is a risk factor for AE-IPF, and the risk-exposure time window related to AE-IPF may lie within 1–2 months before the AE diagnosis. Further investigation is needed on the novel findings regarding the exposure to NO and AE-IPF.
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Literature
1.
go back to reference Raghu G, Collard HR, Egan JJ, Martinez FJ, Behr J, Brown KK, Colby TV, Cordier JF, Flaherty KR, Lasky JA, et al. An official ATS/ERS/JRS/ALAT statement: idiopathic pulmonary fibrosis: evidence-based guidelines for diagnosis and management. Am J Respir Crit Care Med. 2011;183:788–824.CrossRef Raghu G, Collard HR, Egan JJ, Martinez FJ, Behr J, Brown KK, Colby TV, Cordier JF, Flaherty KR, Lasky JA, et al. An official ATS/ERS/JRS/ALAT statement: idiopathic pulmonary fibrosis: evidence-based guidelines for diagnosis and management. Am J Respir Crit Care Med. 2011;183:788–824.CrossRef
2.
go back to reference King TE, Pardo A, Selman M. Idiopathic pulmonary fibrosis. Lancet. 2011;378:1949–61.CrossRef King TE, Pardo A, Selman M. Idiopathic pulmonary fibrosis. Lancet. 2011;378:1949–61.CrossRef
3.
go back to reference Natsuizaka M, Chiba H, Kuronuma K, Otsuka M, Kudo K, Mori M, Bando M, Sugiyama Y, Takahashi H. Epidemiologic survey of Japanese patients with idiopathic pulmonary fibrosis and investigation of ethnic differences. Am J Respir Crit Care Med. 2014;190:773–9.CrossRef Natsuizaka M, Chiba H, Kuronuma K, Otsuka M, Kudo K, Mori M, Bando M, Sugiyama Y, Takahashi H. Epidemiologic survey of Japanese patients with idiopathic pulmonary fibrosis and investigation of ethnic differences. Am J Respir Crit Care Med. 2014;190:773–9.CrossRef
4.
go back to reference Sese L, Nunes H, Cottin V, Sanyal S, Didier M, Carton Z, Israel-Biet D, Crestani B, Cadranel J, Wallaert B, et al. Role of atmospheric pollution on the natural history of idiopathic pulmonary fibrosis. Thorax. 2018;73:145–50.CrossRef Sese L, Nunes H, Cottin V, Sanyal S, Didier M, Carton Z, Israel-Biet D, Crestani B, Cadranel J, Wallaert B, et al. Role of atmospheric pollution on the natural history of idiopathic pulmonary fibrosis. Thorax. 2018;73:145–50.CrossRef
5.
go back to reference King TE Jr, Bradford WZ, Castro-Bernardini S, Fagan EA, Glaspole I, Glassberg MK, Gorina E, Hopkins PM, Kardatzke D, Lancaster L, et al. A phase 3 trial of pirfenidone in patients with idiopathic pulmonary fibrosis. N Engl J Med. 2014;370:2083–92.CrossRef King TE Jr, Bradford WZ, Castro-Bernardini S, Fagan EA, Glaspole I, Glassberg MK, Gorina E, Hopkins PM, Kardatzke D, Lancaster L, et al. A phase 3 trial of pirfenidone in patients with idiopathic pulmonary fibrosis. N Engl J Med. 2014;370:2083–92.CrossRef
6.
go back to reference Richeldi L, du Bois RM, Raghu G, Azuma A, Brown KK, Costabel U, Cottin V, Flaherty KR, Hansell DM, Inoue Y, et al. Efficacy and safety of nintedanib in idiopathic pulmonary fibrosis. N Engl J Med. 2014;370:2071–82.CrossRef Richeldi L, du Bois RM, Raghu G, Azuma A, Brown KK, Costabel U, Cottin V, Flaherty KR, Hansell DM, Inoue Y, et al. Efficacy and safety of nintedanib in idiopathic pulmonary fibrosis. N Engl J Med. 2014;370:2071–82.CrossRef
8.
go back to reference Guenther A, Krauss E, Tello S, Wagner J, Paul B, Kuhn S, Maurer O, Heinemann S, Costabel U, Barbero MAN, et al. The European IPF registry (eurIPFreg): baseline characteristics and survival of patients with idiopathic pulmonary fibrosis. Respir Res. 2018;19:141.CrossRef Guenther A, Krauss E, Tello S, Wagner J, Paul B, Kuhn S, Maurer O, Heinemann S, Costabel U, Barbero MAN, et al. The European IPF registry (eurIPFreg): baseline characteristics and survival of patients with idiopathic pulmonary fibrosis. Respir Res. 2018;19:141.CrossRef
9.
go back to reference Collard HR, Moore BB, Flaherty KR, Brown KK, Kaner RJ, King TE Jr, Lasky JA, Loyd JE, Noth I, Olman MA, et al. Acute exacerbations of idiopathic pulmonary fibrosis. Am J Respir Crit Care Med. 2007;176:636–43.CrossRef Collard HR, Moore BB, Flaherty KR, Brown KK, Kaner RJ, King TE Jr, Lasky JA, Loyd JE, Noth I, Olman MA, et al. Acute exacerbations of idiopathic pulmonary fibrosis. Am J Respir Crit Care Med. 2007;176:636–43.CrossRef
10.
go back to reference Collard HR, Ryerson CJ, Corte TJ, Jenkins G, Kondoh Y, Lederer DJ, Lee JS, Maher TM, Wells AU, Antoniou KM, et al. Acute exacerbation of idiopathic pulmonary fibrosis. An International Working Group Report. Am J Respir Crit Care Med. 2016;194:265–75.CrossRef Collard HR, Ryerson CJ, Corte TJ, Jenkins G, Kondoh Y, Lederer DJ, Lee JS, Maher TM, Wells AU, Antoniou KM, et al. Acute exacerbation of idiopathic pulmonary fibrosis. An International Working Group Report. Am J Respir Crit Care Med. 2016;194:265–75.CrossRef
11.
go back to reference Wootton SC, Kim DS, Kondoh Y, Chen E, Lee JS, Song JW, Huh JW, Taniguchi H, Chiu C, Boushey H, et al. Viral infection in acute exacerbation of idiopathic pulmonary fibrosis. Am J Respir Crit Care Med. 2011;183:1698–702.CrossRef Wootton SC, Kim DS, Kondoh Y, Chen E, Lee JS, Song JW, Huh JW, Taniguchi H, Chiu C, Boushey H, et al. Viral infection in acute exacerbation of idiopathic pulmonary fibrosis. Am J Respir Crit Care Med. 2011;183:1698–702.CrossRef
12.
go back to reference Lee JS, Song JW, Wolters PJ, Elicker BM, King TE Jr, Kim DS, Collard HR. Bronchoalveolar lavage pepsin in acute exacerbation of idiopathic pulmonary fibrosis. Eur Respir J. 2012;39:352–8.CrossRef Lee JS, Song JW, Wolters PJ, Elicker BM, King TE Jr, Kim DS, Collard HR. Bronchoalveolar lavage pepsin in acute exacerbation of idiopathic pulmonary fibrosis. Eur Respir J. 2012;39:352–8.CrossRef
13.
go back to reference Kondoh Y, Taniguchi H, Kitaichi M, Yokoi T, Johkoh T, Oishi T, Kimura T, Nishiyama O, Kato K, du Bois RM. Acute exacerbation of interstitial pneumonia following surgical lung biopsy. Respir Med. 2006;100:1753–9.CrossRef Kondoh Y, Taniguchi H, Kitaichi M, Yokoi T, Johkoh T, Oishi T, Kimura T, Nishiyama O, Kato K, du Bois RM. Acute exacerbation of interstitial pneumonia following surgical lung biopsy. Respir Med. 2006;100:1753–9.CrossRef
14.
go back to reference Johannson KA, Vittinghoff E, Lee K, Balmes JR, Ji W, Kaplan GG, Kim DS, Collard HR. Acute exacerbation of idiopathic pulmonary fibrosis associated with air pollution exposure. Eur Respir J. 2014;43:1124–2113.CrossRef Johannson KA, Vittinghoff E, Lee K, Balmes JR, Ji W, Kaplan GG, Kim DS, Collard HR. Acute exacerbation of idiopathic pulmonary fibrosis associated with air pollution exposure. Eur Respir J. 2014;43:1124–2113.CrossRef
15.
go back to reference Brunekreef B, Holgate ST. Air pollution and health. Lancet. 2002;360:1233–42.CrossRef Brunekreef B, Holgate ST. Air pollution and health. Lancet. 2002;360:1233–42.CrossRef
16.
go back to reference Dominici F, Peng RD, Bell ML, Pham L, McDermott A, Zeger SL, Samet JM. Fine particulate air pollution and hospital admission for cardiovascular and respiratory diseases. JAMA. 2006;295:1127–34.CrossRef Dominici F, Peng RD, Bell ML, Pham L, McDermott A, Zeger SL, Samet JM. Fine particulate air pollution and hospital admission for cardiovascular and respiratory diseases. JAMA. 2006;295:1127–34.CrossRef
17.
go back to reference Atkinson RW, Kang S, Anderson HR, Mills IC, Walton HA. Epidemiological time series studies of PM2.5 and daily mortality and hospital admissions: a systematic review and meta-analysis. Thorax. 2014;69:660–5.CrossRef Atkinson RW, Kang S, Anderson HR, Mills IC, Walton HA. Epidemiological time series studies of PM2.5 and daily mortality and hospital admissions: a systematic review and meta-analysis. Thorax. 2014;69:660–5.CrossRef
18.
go back to reference Li MH, Fan LC, Mao B, Yang JW, Choi AMK, Cao WJ, Xu JF. Short-term exposure to ambient fine particulate matter increases hospitalizations and mortality in COPD: a systematic review and meta-analysis. Chest. 2016;149:447–58.CrossRef Li MH, Fan LC, Mao B, Yang JW, Choi AMK, Cao WJ, Xu JF. Short-term exposure to ambient fine particulate matter increases hospitalizations and mortality in COPD: a systematic review and meta-analysis. Chest. 2016;149:447–58.CrossRef
19.
go back to reference Dales R, Blanco-Vidal C, Cakmak S. The association between air pollution and hospitalization of patients with idiopathic pulmonary fibrosis in chile: a daily time series analysis. Chest. 2020;158:630–6.CrossRef Dales R, Blanco-Vidal C, Cakmak S. The association between air pollution and hospitalization of patients with idiopathic pulmonary fibrosis in chile: a daily time series analysis. Chest. 2020;158:630–6.CrossRef
20.
go back to reference Fujisawa T, Mori K, Mikamo M, Ohno T, Kataoka K, Sugimoto C, Kitamura H, Enomoto N, Egashira R, Sumikawa H, et al. Nationwide cloud-based integrated database of idiopathic interstitial pneumonias for multidisciplinary discussion. Eur Respir J. 2019;53:1802243.CrossRef Fujisawa T, Mori K, Mikamo M, Ohno T, Kataoka K, Sugimoto C, Kitamura H, Enomoto N, Egashira R, Sumikawa H, et al. Nationwide cloud-based integrated database of idiopathic interstitial pneumonias for multidisciplinary discussion. Eur Respir J. 2019;53:1802243.CrossRef
21.
go back to reference Diez-Roux AV. Multilevel analysis in public health research. Annu Rev Public Health. 2000;21:171–92.CrossRef Diez-Roux AV. Multilevel analysis in public health research. Annu Rev Public Health. 2000;21:171–92.CrossRef
22.
go back to reference Navidi W, Thomas D, Stram D, Peters J. Design and analysis of multilevel analytic studies with applications to a study of air pollution. Environ Health Perspect. 1994;102(Suppl 8):25–32.CrossRef Navidi W, Thomas D, Stram D, Peters J. Design and analysis of multilevel analytic studies with applications to a study of air pollution. Environ Health Perspect. 1994;102(Suppl 8):25–32.CrossRef
23.
go back to reference Carracedo-Martinez E, Taracido M, Tobias A, Saez M, Figueiras A. Case-crossover analysis of air pollution health effects: a systematic review of methodology and application. Environ Health Perspect. 2010;118:1173–82.CrossRef Carracedo-Martinez E, Taracido M, Tobias A, Saez M, Figueiras A. Case-crossover analysis of air pollution health effects: a systematic review of methodology and application. Environ Health Perspect. 2010;118:1173–82.CrossRef
24.
go back to reference American Thoracic S, European Respiratory S: American Thoracic Society/European Respiratory Society International Multidisciplinary Consensus Classification of the Idiopathic Interstitial Pneumonias. This joint statement of the American Thoracic Society (ATS), and the European Respiratory Society (ERS) was adopted by the ATS board of directors, June 2001 and by the ERS Executive Committee, June 2001. Am J Respir Crit Care Med 2002;165:277–304. American Thoracic S, European Respiratory S: American Thoracic Society/European Respiratory Society International Multidisciplinary Consensus Classification of the Idiopathic Interstitial Pneumonias. This joint statement of the American Thoracic Society (ATS), and the European Respiratory Society (ERS) was adopted by the ATS board of directors, June 2001 and by the ERS Executive Committee, June 2001. Am J Respir Crit Care Med 2002;165:277–304.
25.
go back to reference Travis WD, Costabel U, Hansell DM, King TE, Jr., Lynch DA, Nicholson AG, Ryerson CJ, Ryu JH, Selman M, Wells AU, et al: An official American Thoracic Society/European Respiratory Society statement: Update of the international multidisciplinary classification of the idiopathic interstitial pneumonias. 2013;188:733–748 Travis WD, Costabel U, Hansell DM, King TE, Jr., Lynch DA, Nicholson AG, Ryerson CJ, Ryu JH, Selman M, Wells AU, et al: An official American Thoracic Society/European Respiratory Society statement: Update of the international multidisciplinary classification of the idiopathic interstitial pneumonias. 2013;188:733–748
26.
go back to reference Song JW, Hong SB, Lim CM, Koh Y, Kim DS. Acute exacerbation of idiopathic pulmonary fibrosis: incidence, risk factors and outcome. Eur Respir J. 2011;37:356–63.CrossRef Song JW, Hong SB, Lim CM, Koh Y, Kim DS. Acute exacerbation of idiopathic pulmonary fibrosis: incidence, risk factors and outcome. Eur Respir J. 2011;37:356–63.CrossRef
27.
go back to reference Bowe B, Xie Y, Yan Y, Al-Aly Z. Burden of cause-specific mortality associated with PM2.5 air pollution in the United States. JAMA Netw Open. 2019;2:e1915834.CrossRef Bowe B, Xie Y, Yan Y, Al-Aly Z. Burden of cause-specific mortality associated with PM2.5 air pollution in the United States. JAMA Netw Open. 2019;2:e1915834.CrossRef
28.
go back to reference Falcon-Rodriguez CI, Osornio-Vargas AR, Sada-Ovalle I, Segura-Medina P. Aeroparticles, composition, and lung diseases. Front Immunol. 2016;7:3.CrossRef Falcon-Rodriguez CI, Osornio-Vargas AR, Sada-Ovalle I, Segura-Medina P. Aeroparticles, composition, and lung diseases. Front Immunol. 2016;7:3.CrossRef
29.
go back to reference Nel AE, Diaz-Sanchez D, Ng D, Hiura T, Saxon A. Enhancement of allergic inflammation by the interaction between diesel exhaust particles and the immune system. J Allergy Clin Immunol. 1998;102:539–54.CrossRef Nel AE, Diaz-Sanchez D, Ng D, Hiura T, Saxon A. Enhancement of allergic inflammation by the interaction between diesel exhaust particles and the immune system. J Allergy Clin Immunol. 1998;102:539–54.CrossRef
30.
go back to reference Nel A. Atmosphere. Air pollution-related illness: effects of particles. Science. 2005;308:804–6.CrossRef Nel A. Atmosphere. Air pollution-related illness: effects of particles. Science. 2005;308:804–6.CrossRef
31.
go back to reference Gilliland FD, Li YF, Saxon A, Diaz-Sanchez D. Effect of glutathione-S-transferase M1 and P1 genotypes on xenobiotic enhancement of allergic responses: randomised, placebo-controlled crossover study. Lancet. 2004;363:119–25.CrossRef Gilliland FD, Li YF, Saxon A, Diaz-Sanchez D. Effect of glutathione-S-transferase M1 and P1 genotypes on xenobiotic enhancement of allergic responses: randomised, placebo-controlled crossover study. Lancet. 2004;363:119–25.CrossRef
32.
go back to reference Mukae H, Vincent R, Quinlan K, English D, Hards J, Hogg JC, van Eeden SF. The effect of repeated exposure to particulate air pollution (PM10) on the bone marrow. Am J Respir Crit Care Med. 2001;163:201–9.CrossRef Mukae H, Vincent R, Quinlan K, English D, Hards J, Hogg JC, van Eeden SF. The effect of repeated exposure to particulate air pollution (PM10) on the bone marrow. Am J Respir Crit Care Med. 2001;163:201–9.CrossRef
33.
go back to reference North CM, Rice MB, Ferkol T, Gozal D, Hui C, Jung SH, Kuribayashi K, McCormack MC, Mishima M, Morimoto Y, et al. Air pollution in the Asia-Pacific Region: A Joint Asian Pacific Society of Respirology/American Thoracic Society perspective (Republication). Respirology. 2019;24:484–91.CrossRef North CM, Rice MB, Ferkol T, Gozal D, Hui C, Jung SH, Kuribayashi K, McCormack MC, Mishima M, Morimoto Y, et al. Air pollution in the Asia-Pacific Region: A Joint Asian Pacific Society of Respirology/American Thoracic Society perspective (Republication). Respirology. 2019;24:484–91.CrossRef
34.
go back to reference Europe, W. H. O. R. O. for & Organization, W. H. Air Quality Guidelines: Global update 2005: Particulate matter, ozone, nitrogen dioxide and sulfur dioxide. World Health Organization, 2006 Europe, W. H. O. R. O. for & Organization, W. H. Air Quality Guidelines: Global update 2005: Particulate matter, ozone, nitrogen dioxide and sulfur dioxide. World Health Organization, 2006
35.
go back to reference Raghu G, Remy-Jardin M, Myers JL, Richeldi L, Ryerson CJ, Lederer DJ, Behr J, Cottin V, Danoff SK, Morell F, et al. Diagnosis of idiopathic pulmonary fibrosis. An official ATS/ERS/JRS/ALAT clinical practice guideline. Am J Respir Crit Care Med. 2018;198:44–68.CrossRef Raghu G, Remy-Jardin M, Myers JL, Richeldi L, Ryerson CJ, Lederer DJ, Behr J, Cottin V, Danoff SK, Morell F, et al. Diagnosis of idiopathic pulmonary fibrosis. An official ATS/ERS/JRS/ALAT clinical practice guideline. Am J Respir Crit Care Med. 2018;198:44–68.CrossRef
36.
go back to reference Raghu G, Mageto YN, Lockhart D, Schmidt RA, Wood DE, Godwin JD. The accuracy of the clinical diagnosis of new-onset idiopathic pulmonary fibrosis and other interstitial lung disease: a prospective study. Chest. 1999;116:1168–74.CrossRef Raghu G, Mageto YN, Lockhart D, Schmidt RA, Wood DE, Godwin JD. The accuracy of the clinical diagnosis of new-onset idiopathic pulmonary fibrosis and other interstitial lung disease: a prospective study. Chest. 1999;116:1168–74.CrossRef
37.
go back to reference Hunninghake GW, Zimmerman MB, Schwartz DA, King TE Jr, Lynch J, Hegele R, Waldron J, Colby T, Muller N, Lynch D, et al. Utility of a lung biopsy for the diagnosis of idiopathic pulmonary fibrosis. Am J Respir Crit Care Med. 2001;164:193–6.CrossRef Hunninghake GW, Zimmerman MB, Schwartz DA, King TE Jr, Lynch J, Hegele R, Waldron J, Colby T, Muller N, Lynch D, et al. Utility of a lung biopsy for the diagnosis of idiopathic pulmonary fibrosis. Am J Respir Crit Care Med. 2001;164:193–6.CrossRef
38.
go back to reference Lederer DJ, Martinez FJ. Idiopathic pulmonary fibrosis. N Engl J Med. 2018;378:1811–23.CrossRef Lederer DJ, Martinez FJ. Idiopathic pulmonary fibrosis. N Engl J Med. 2018;378:1811–23.CrossRef
Metadata
Title
Exposure to PM2.5 is a risk factor for acute exacerbation of surgically diagnosed idiopathic pulmonary fibrosis: a case–control study
Authors
Masahiro Tahara
Yoshihisa Fujino
Kei Yamasaki
Keishi Oda
Takashi Kido
Noriho Sakamoto
Toshinori Kawanami
Kensuke Kataoka
Ryoko Egashira
Mikiko Hashisako
Yuzo Suzuki
Tomoyuki Fujisawa
Hiroshi Mukae
Takafumi Suda
Kazuhiro Yatera
Publication date
01-12-2021
Publisher
BioMed Central
Published in
Respiratory Research / Issue 1/2021
Electronic ISSN: 1465-993X
DOI
https://doi.org/10.1186/s12931-021-01671-6

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