Does a Type of Inciting Antigen Correlate with the Presence of Lung Fibrosis in Patients with Hypersensitivity Pneumonitis?
Abstract
:1. Introduction
2. Materials and Methods
2.1. Study Group
2.2. Questionnaire
2.3. Precipitins
2.4. High-Resolution CT Scan (HRCT)
2.5. BAL Fluid Cellular Analysis
2.6. Statistical Analysis
2.7. Regulatory Board Approval
3. Results
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Kaul, B.; Cottin, V.; Collard, H.R.; Valenzuela, C. Variability in Global Prevalence of Interstitial Lung Disease. Front. Med. 2021, 8, 1971. [Google Scholar] [CrossRef]
- Raghu, G.; Remy-Jardin, M.; Ryerson, C.J.; Myers, J.L.; Kreuter, M.; Vasakova, M.; Bargagli, E.; Chung, J.H.; Collins, B.F.; Bendstrup, E.; et al. Diagnosis of Hypersensitivity Pneumonitis in Adults. An Official ATS/JRS/ALAT Clinical Practice Guideline. Am. J. Respir. Crit. Care Med. 2020, 202, e36–e69. [Google Scholar] [CrossRef]
- Fernández Pérez, E.R.; Travis, W.D.; Lynch, D.A.; Brown, K.K.; Johannson, K.A.; Selman, M.; Ryu, J.H.; Wells, A.U.; Tony Huang, Y.-C.; Pereira, C.A.C.; et al. Diagnosis and Evaluation of Hypersensitivity Pneumonitis. Chest 2021, 160, e97–e156. [Google Scholar] [CrossRef] [PubMed]
- Vasakova, M.; Morell, F.; Walsh, S.; Leslie, K.; Raghu, G. Hypersensitivity Pneumonitis: Perspectives in Diagnosis and Management. Am. J. Respir. Crit. Care Med. 2017, 196, 680–689. [Google Scholar] [CrossRef] [PubMed]
- Barnes, H.; Morisset, J.; Molyneaux, P.; Westall, G.; Glaspole, I.; Collard, H.R.; CHP Exposure Assessment Collaborators. A Systematically Derived Exposure Assessment Instrument for Chronic Hypersensitivity Pneumonitis. Chest 2020, 157, 1506–1512. [Google Scholar] [CrossRef]
- Lee, C.T.; Strek, M.E.; Adegunsoye, A.; Wong, A.W.; Assayag, D.; Cox, G.; Fell, C.D.; Fisher, J.H.; Gershon, A.S.; Halayko, A.J.; et al. Inhalational exposures in patients with fibrotic interstitial lung disease: Presentation, pulmonary function and survival in the Canadian Registry for Pulmonary Fibrosis. Respirology 2022, 27, 635–644. [Google Scholar] [CrossRef]
- Szturmowicz, M.; Garczewska, B.; Jędrych, M.E.; Bartoszuk, I.; Sobiecka, M.; Tomkowski, W.; Augustynowicz-Kopeć, E. The value of serum precipitins against specific antigens in patients diagnosed with hypersensitivity pneumonitis—Retrospective study. Cent. Eur. J. Immunol. 2019, 44, 390–394. [Google Scholar] [CrossRef]
- Simpson, C.; Shirodaria, P.V.; Evans, J.P.; Simpson, D.I.; Stanford, C.F. Comparison of immunodiffusion and enzyme linked immunosorbent assay in the detection of abnormal antibodies in pigeon breeder’s disease. J. Clin. Pathol. 1992, 45, 490–493. [Google Scholar] [CrossRef] [PubMed]
- Suhara, K.; Miyazaki, Y.; Okamoto, T.; Yasui, M.; Tsuchiya, K.; Inase, N. Utility of immunological tests for bird-related hypersensitivity pneumonitis. Respir. Investig. 2015, 53, 13–21. [Google Scholar] [CrossRef]
- Meleniewska-Maciszewska, A. Usefulness of antigens isolated from pigeon droppings for serological tests in he diagnosis of extrinsic allergic alveolitis in pigeon breeders. Pneumonol. Pol. 1980, 48, 609–617. [Google Scholar]
- Okuda, R.; Takemura, T.; Mikami, Y.; Hagiwara, E.; Iwasawa, T.; Baba, T.; Kitamura, H.; Komatsu, S.; Okudela, K.; Ohashi, K.; et al. Inhalation challenge test using pigeon eggs for chronic hypersensitivity pneumonitis. Clin. Exp. Allergy 2020, 50, 1381–1390. [Google Scholar] [CrossRef] [PubMed]
- Shiroshita, A.; Jin, Z.; Tanaka, Y.; Kataoka, Y. Diagnostic accuracy and safety of inhalation challenge tests for bird fancier’s lung-Systematic review and meta-analysis. Clin. Exp. Allergy 2020, 50, 1007–1016. [Google Scholar] [CrossRef]
- Raghu, G.; Remy-Jardin, M.; Richeldi, L.; Thomson, C.C.; Inoue, Y.; Johkoh, T.; Kreuter, M.; Lynch, D.A.; Maher, T.M.; Martinez, F.J.; et al. Idiopathic Pulmonary Fibrosis (an Update) and Progressive Pulmonary Fibrosis in Adults: An Official ATS/ERS/JRS/ALAT Clinical Practice Guideline. Am. J. Respir. Crit. Care Med. 2022, 205, e18–e47. [Google Scholar] [CrossRef]
- Morell, F.; Villar, A.; Montero, M.-Á.; Muñoz, X.; Colby, T.V.; Pipvath, S.; Cruz, M.-J.; Raghu, G. Chronic hypersensitivity pneumonitis in patients diagnosed with idiopathic pulmonary fibrosis: A prospective case-cohort study. Lancet Respir. Med. 2013, 1, 685–694. [Google Scholar] [CrossRef]
- Fernández Pérez, E.R.; Swigris, J.J.; Forssén, A.V.; Tourin, O.; Solomon, J.J.; Huie, T.J.; Olson, A.L.; Brown, K.K. Identifying an inciting antigen is associated with improved survival in patients with chronic hypersensitivity pneumonitis. Chest 2013, 144, 1644–1651. [Google Scholar] [CrossRef]
- Sobiecka, M.; Szturmowicz, M.; Lewandowska, K.B.; Barańska, I.; Zimna, K.; Łyżwa, E.; Dybowska, M.; Langfort, R.; Radwan-Röhrenschef, P.; Roży, A.; et al. Bronchoalveolar Lavage Cell Count and Lymphocytosis Are the Important Discriminators between Fibrotic Hypersensitivity Pneumonitis and Idiopathic Pulmonary Fibrosis. Diagnostics 2023, 13, 935. [Google Scholar] [CrossRef]
- Baughman, R.P. Technical aspects of bronchoalveolar lavage: Recommendations for a standard procedure. Semin. Respir. Crit. Care Med. 2007, 28, 475–485. [Google Scholar] [CrossRef]
- Lewandowska, K.B.; Barańska, I.; Sobiecka, M.; Radwan-Rohrenschef, P.; Dybowska, M.; Franczuk, M.; Roży, A.; Skoczylas, A.; Bestry, I.; Kuś, J.; et al. Factors Predictive for Immunomodulatory Therapy Response and Survival in Patients with Hypersensitivity Pneumonitis-Retrospective Cohort Analysis. Diagnostics 2022, 12, 2767. [Google Scholar] [CrossRef]
- Vourlekis, J.S.; Schwarz, M.I.; Cherniack, R.M.; Curran-Everett, D.; Cool, C.D.; Tuder, R.M.; King, T.E.; Brown, K.K. The effect of pulmonary fibrosis on survival in patients with hypersensitivity pneumonitis. Am. J. Med. 2004, 116, 662–668. [Google Scholar] [CrossRef]
- Salisbury, M.L.; Gu, T.; Murray, S.; Gross, B.H.; Chughtai, A.; Sayyouh, M.; Kazerooni, E.A.; Myers, J.L.; Lagstein, A.; Konopka, K.E.; et al. Hypersensitivity Pneumonitis: Radiologic Phenotypes Are Associated with Distinct Survival Time and Pulmonary Function Trajectory. Chest 2019, 155, 699–711. [Google Scholar] [CrossRef]
- Vasakova, M.; Selman, M.; Morell, F.; Sterclova, M.; Molina-Molina, M.; Raghu, G. Hypersensitivity Pneumonitis: Current Concepts of Pathogenesis and Potential Targets for Treatment. Am. J. Respir. Crit. Care Med. 2019, 200, 301–308. [Google Scholar] [CrossRef]
- Hamblin, M.; Prosch, H.; Vašáková, M. Diagnosis, course and management of hypersensitivity pneumonitis. Eur. Respir. Rev. 2022, 31, 210169. [Google Scholar] [CrossRef]
- Barnes, H.; Chambers, D.; Grainge, C.; Corte, T.J.; Bastiampillai, S.; Frenkel, S.; Westall, G.; Collard, H.; Glaspole, I. Clinical utility of a standardized chronic hypersensitivity pneumonitis exposure questionnaire. Respirology 2023, 28, 366–372. [Google Scholar] [CrossRef]
- Pohle, S.; Guler, S.A.; Hostettler, K.E.; Clarenbach, C.; Fellrath, J.-M.; Azzola, A.; Adler, D.; Scholtze, D.; Pavlov, N.; Ulrich, S.; et al. Swiss Hypersensitivity Pneumonitis Exposure Questionnaire: A Regionally Adapted and Easy-To-Use Aide for Patients and Clinicians. Respiration 2023, 102, 465–468. [Google Scholar] [CrossRef] [PubMed]
- Polke, M.; Kirsten, D.; Teucher, B.; Kahn, N.; Geissler, K.; Costabel, U.; Herth, F.J.F.; Kreuter, M. A Comparison of Existing Questionnaires for Identifying the Causes of Interstitial and Rare Lung Diseases. Respiration 2020, 99, 119–124. [Google Scholar] [CrossRef]
- Spagnolo, P.; Ryerson, C.J.; Guler, S.; Feary, J.; Churg, A.; Fontenot, A.P.; Piciucchi, S.; Udwadia, Z.; Corte, T.J.; Wuyts, W.A.; et al. Occupational interstitial lung diseases. J. Intern. Med. 2023, 294, 798–815. [Google Scholar] [CrossRef] [PubMed]
- Barnes, H.; Lu, J.; Glaspole, I.; Collard, H.R.; Johannson, K.A. Exposures and associations with clinical phenotypes in hypersensitivity pneumonitis: A scoping review. Respir. Med. 2021, 184, 106444. [Google Scholar] [CrossRef] [PubMed]
- Tomioka, H.; Miyazaki, Y.; Inoue, Y.; Egashira, R.; Kawamura, T.; Sano, H.; Johkoh, T.; Takemura, T.; Hisada, T.; Fukuoka, J.; et al. Japanese clinical practice guide 2022 for hypersensitivity pneumonitis. Respir. Investig. 2024, 62, 16–43. [Google Scholar] [CrossRef]
- Adams, T.N.; Newton, C.A.; Glazer, C.S. Role of Antigen Type in Survival in Chronic Hypersensitivity Pneumonitis. Lung 2019, 197, 113–114. [Google Scholar] [CrossRef]
- De Sadeleer, L.J.; Hermans, F.; De Dycker, E.; Yserbyt, J.; Verschakelen, J.A.; Verbeken, E.K.; Verleden, G.M.; Wuyts, W.A. Effects of Corticosteroid Treatment and Antigen Avoidance in a Large Hypersensitivity Pneumonitis Cohort: A Single-Centre Cohort Study. J. Clin. Med. 2018, 8, 14. [Google Scholar] [CrossRef]
- Nishida, T.; Kawate, E.; Ishiguro, T.; Kanauchi, T.; Shimizu, Y.; Takayanagi, N. Antigen avoidance and outcome of nonfibrotic and fibrotic hypersensitivity pneumonitis. ERJ Open Res. 2022, 8, 00474-02021. [Google Scholar] [CrossRef]
- Petnak, T.; Thongprayoon, C.; Baqir, M.; Ryu, J.H.; Moua, T. Antigen identification and avoidance on outcomes in fibrotic hypersensitivity pneumonitis. Eur. Respir. J. 2022, 60, 2101336. [Google Scholar] [CrossRef] [PubMed]
- Okuda, R.; Takemura, T.; Iwasawa, T.; Kaburaki, S.; Baba, T.; Hagiwara, E.; Ogura, T. Impact of antigen avoidance test for fibrotic hypersensitivity pneumonitis in stable phase. Allergy Asthma Clin. Immunol. 2022, 18, 104. [Google Scholar] [CrossRef] [PubMed]
- Hanak, V.; Golbin, J.M.; Hartman, T.E.; Ryu, J.H. High-Resolution CT Findings of Parenchymal Fibrosis Correlate with Prognosis in Hypersensitivity Pneumonitis. Chest 2008, 134, 133–138. [Google Scholar] [CrossRef] [PubMed]
- Lyons, S.; Mao, L.; Nolan, A.; O’Sullivan, V. The effect of “smoky” coal bans on chronic lung disease among older people in Ireland. Econ. Hum. Biol. 2023, 50, 101275. [Google Scholar] [CrossRef]
- Wuyts, W.; Sterclova, M.; Vasakova, M. Pitfalls in diagnosis and management of hypersensitivity pneumonitis. Curr. Opin. Pulm. Med. 2015, 21, 490–498. [Google Scholar] [CrossRef]
- Jenkins, A.R.; Chua, A.; Chami, H.; Diaz-Mendoza, J.; Duggal, A.; Knight, S.; Patolia, S.; Tamae-Kakazu, M.; Raghu, G.; Wilson, K.C. Questionnaires or Serum Immunoglobulin G Testing in the Diagnosis of Hypersensitivity Pneumonitis among Patients with Interstitial Lung Disease. Ann. Am. Thorac. Soc. 2021, 18, 130–147. [Google Scholar] [CrossRef]
- Raghu, G.; Chen, S.-Y.; Hou, Q.; Yeh, W.-S.; Collard, H.R. Incidence and prevalence of idiopathic pulmonary fibrosis in US adults 18–64 years old. Eur. Respir. J. 2016, 48, 179–186. [Google Scholar] [CrossRef]
- Parimon, T.; Hohmann, M.S.; Yao, C. Cellular Senescence: Pathogenic Mechanisms in Lung Fibrosis. Int. J. Mol. Sci. 2021, 22, 6214. [Google Scholar] [CrossRef]
- Morell, F.; Roger, À.; Reyes, L.; Cruz, M.J.; Murio, C.; Muñoz, X. Bird fancier’s lung: A series of 86 patients. Medicine 2008, 87, 110–130. [Google Scholar] [CrossRef]
- Ejima, M.; Okamoto, T.; Suzuki, T.; Anzai, T.; Takahashi, K.; Miyazaki, Y. Efficacy of treatment with corticosteroids for fibrotic hypersensitivity pneumonitis: A propensity score-matched cohort analysis. BMC Pulm. Med. 2021, 21, 243. [Google Scholar] [CrossRef]
- De Sadeleer, L.J.; Hermans, F.; De Dycker, E.; Yserbyt, J.; Verschakelen, J.A.; Verbeken, E.K.; Verleden, G.M.; Verleden, S.E.; Wuyts, W.A. Impact of BAL lymphocytosis and presence of honeycombing on corticosteroid treatment effect in fibrotic hypersensitivity pneumonitis: A retrospective cohort study. Eur. Respir. J. 2020, 55, 1901983. [Google Scholar] [CrossRef] [PubMed]
- Adams, T.N.; Newton, C.A.; Batra, K.; Abu-Hijleh, M.; Barbera, T.; Torrealba, J.; Glazer, C.S. Utility of Bronchoalveolar Lavage and Transbronchial Biopsy in Patients with Hypersensitivity Pneumonitis. Lung 2018, 196, 617–622. [Google Scholar] [CrossRef] [PubMed]
Parameter | Whole Group, N = 66 | F-HP, N = 46 | Non-fHP, N = 20 | p |
---|---|---|---|---|
Age at diagnosis, median (IQR) | 59 (46.75–67) | 60 (47.75–68.25) | 52.5 (43.25–63.75) | 0.06 |
Male sex, n (%) | 27 (40.9) | 18 (39.1) | 9 (45) | 0.77 |
Ever smoker, n (%) | 15 (22.7) | 8 (17.4) | 7 (35) | 0.19 |
BAL lymph (%), median, (IQR) | 38.8 (26.9–52.6) | 35.85 (23.14–48.25) | 51 (36.6–66.6) | 0.007 |
Time from symptom onset to HP diagnosis (months), median (IQR) | 24 (11.25–63.00) | 36 (12–75) | 24 (6.25–60.00 | 0.2 |
Parameter | Whole Group, N = 66 | F-HP, N = 46 | Non-fHP, N = 20 | p |
---|---|---|---|---|
Antigen exposures reported in the questionnaire, n (%) | 62 (93.9) | 43 (93.75) | 19 (95.0) | >0.99 |
Number of antigens, median (IQR) | 3 (2–4.25) | 3 (2–5) | 2 (1.25–4) | 0.09 |
type of antigen | ||||
Poultry, n (%) | 29 (43.9) | 23 (50) | 6 (31.6) | 0.27 |
Farming, n (%) | 29 (43.9) | 19 (41.3) | 10 (50) | 0.51 |
Pigeons, n (%) | 20 (30.3) | 16 (34.8) | 4 (20) | 0.23 |
Feather duvets, n (%) | 30 (45.5) | 23 (50) | 7 (35) | 0.29 |
Molds, n (%) | 24 (36.4) | 18 (31.9) | 6 (30) | 0.58 |
Water systems, n (%) | 36 (54.5) | 25 (54.35) | 11 (55) | >0.99 |
Biomass/coal heating, n (%) | 13 (20.3) | 12 (27.3) | 1 (5) | 0.05 |
Occupational exposures, n (%) | 17 (25.75) | 12 (26) | 5 (25) | >0.99 |
Any avian (poultry, pigeons, other birds), n (%) | 40 (60.6) | 32 (69.6) | 8 (40) | 0.03 |
Positive precipitins (any), n (%) | 30 (46.9) | 23 (51.1) | 7 (36.8) | 0.41 |
Positive avian precipitins, n (%) | 28 (47.5) | 23 (56.1) | 5 (27.8) | 0.05 |
Positive precipitins against thermophilic actinomycetes (farmer’s lung), n (%) | 8 (12.9) | 4 (9.3) | 4 (21.1) | 0.21 |
Variable | OR | 95% CI (Profile Likelihood) | p Value |
---|---|---|---|
Lymph in BAL (%) | 0.9694 | 0.9336–1.003 | 0.08 |
Age at diagnosis | 1.064 | 1.004–1.138 | 0.04 |
Smoking | 0.2712 | 0.051–1.281 | 0.11 |
Coal heating | 1.693 | 0.2054–36.37 | 0.66 |
Farming | 0.5749 | 0.1259–2.450 | 0.46 |
Avian antigens | 1.928 | 0.4336–9.237 | 0.39 |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2024 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Deutsch, K.; Lewandowska, K.B.; Kowalik, A.; Bartoszuk, I.; Radwan-Röhrenschef, P.; Sobiecka, M.; Dybowska, M.; Tomkowski, W.Z.; Szturmowicz, M. Does a Type of Inciting Antigen Correlate with the Presence of Lung Fibrosis in Patients with Hypersensitivity Pneumonitis? J. Clin. Med. 2024, 13, 5074. https://doi.org/10.3390/jcm13175074
Deutsch K, Lewandowska KB, Kowalik A, Bartoszuk I, Radwan-Röhrenschef P, Sobiecka M, Dybowska M, Tomkowski WZ, Szturmowicz M. Does a Type of Inciting Antigen Correlate with the Presence of Lung Fibrosis in Patients with Hypersensitivity Pneumonitis? Journal of Clinical Medicine. 2024; 13(17):5074. https://doi.org/10.3390/jcm13175074
Chicago/Turabian StyleDeutsch, Kamila, Katarzyna B. Lewandowska, Agata Kowalik, Iwona Bartoszuk, Piotr Radwan-Röhrenschef, Małgorzata Sobiecka, Małgorzata Dybowska, Witold Z. Tomkowski, and Monika Szturmowicz. 2024. "Does a Type of Inciting Antigen Correlate with the Presence of Lung Fibrosis in Patients with Hypersensitivity Pneumonitis?" Journal of Clinical Medicine 13, no. 17: 5074. https://doi.org/10.3390/jcm13175074