A prospective cohort study of periostin as a serum biomarker in patients with idiopathic pulmonary fibrosis treated with nintedanib.


Journal

Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288

Informations de publication

Date de publication:
27 Dec 2023
Historique:
received: 27 04 2023
accepted: 05 12 2023
medline: 28 12 2023
pubmed: 28 12 2023
entrez: 27 12 2023
Statut: epublish

Résumé

This study investigated the utility of periostin, a matricellular protein, as a prognostic biomarker in patients with idiopathic pulmonary fibrosis (IPF) who received nintedanib. Monomeric and total periostin levels were measured by enzyme-linked immunosorbent assay in 87 eligible patients who participated in a multicenter prospective study. Forty-three antifibrotic drug-naive patients with IPF described in previous studies were set as historical controls. Monomeric and total periostin levels were not significantly associated with the change in forced vital capacity (FVC) or diffusing capacity of the lungs for carbon monoxide (D

Identifiants

pubmed: 38151520
doi: 10.1038/s41598-023-49180-4
pii: 10.1038/s41598-023-49180-4
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

22977

Subventions

Organisme : Grant-in-Aid for Scientific Research
ID : 19K08637

Informations de copyright

© 2023. The Author(s).

Références

Raghu, G. 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. 205, e18–e47 (2022).
pubmed: 35486072 pmcid: 9851481 doi: 10.1164/rccm.202202-0399ST
Raghu, G. et al. Diagnosis of idiopathic pulmonary fibrosis. An official ATS/ERS/JRS/ALAT clinical practice guideline. Am. J. Respir. Crit. Care Med. 198, 44–68 (2018).
doi: 10.1164/rccm.201807-1255ST
Raghu, G. 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. 183, 788–824 (2011).
pubmed: 21471066 pmcid: 5450933 doi: 10.1164/rccm.2009-040GL
Natsuizaka, M. et al. Epidemiologic survey of Japanese patients with idiopathic pulmonary fibrosis and investigation of ethnic differences. Am. J. Respir. Crit. Care Med. 190, 773–779 (2014).
pubmed: 25162152 doi: 10.1164/rccm.201403-0566OC
Flaherty, K. R. et al. Prognostic implications of physiologic and radiographic changes in idiopathic interstitial pneumonia. Am. J. Respir. Crit. Care Med. 168, 543–548 (2003).
pubmed: 12773329 doi: 10.1164/rccm.200209-1112OC
Zappala, C. J. et al. Marginal decline in forced vital capacity is associated with a poor outcome in idiopathic pulmonary fibrosis. Eur. Respir. J. 35, 830–836 (2010).
pubmed: 19840957 doi: 10.1183/09031936.00155108
Latsi, P. I. et al. Fibrotic idiopathic interstitial pneumonia: The prognostic value of longitudinal functional trends. Am. J. Respir. Crit. Care Med. 168, 531–537 (2003).
pubmed: 12791580 doi: 10.1164/rccm.200210-1245OC
Mogulkoc, N. et al. Greater Manchester Pulmonary Fibrosis Consortium. Pulmonary function in idiopathic pulmonary fibrosis and referral for lung transplantation. Am. J. Respir. Crit. Care Med. 164, 103–108 (2001).
pubmed: 11435247 doi: 10.1164/ajrccm.164.1.2007077
Richeldi, L. et al. Efficacy and safety of nintedanib in idiopathic pulmonary fibrosis. N. Engl. J. Med. 370, 2071–2082 (2014).
pubmed: 24836310 doi: 10.1056/NEJMoa1402584
King, T. E. Jr. et al. A phase 3 trial of pirfenidone in patients with idiopathic pulmonary fibrosis. N. Engl. J. Med. 370, 2083–2092 (2014).
pubmed: 24836312 doi: 10.1056/NEJMoa1402582
Petnak, T., Lertjitbanjong, P., Thongprayoon, C. & Moua, T. Impact of antifibrotic therapy on mortality and acute exacerbation in idiopathic pulmonary fibrosis: A systematic review and meta-analysis. Chest 160, 1751–1763 (2021).
pubmed: 34217681 doi: 10.1016/j.chest.2021.06.049
Homma, S. et al. Japanese guideline for the treatment of idiopathic pulmonary fibrosis. Respir Investig. 56, 268–291 (2018).
pubmed: 29980444 doi: 10.1016/j.resinv.2018.03.003
Ley, B. et al. Predictors of mortality poorly predict common measures of disease progression in idiopathic pulmonary fibrosis. Am. J. Respir. Crit. Care Med. 194, 711–718 (2016).
pubmed: 26938706 pmcid: 5027229 doi: 10.1164/rccm.201508-1546OC
Ryerson, C. J. et al. Predicting survival across chronic interstitial lung disease: The ILD-GAP model. Chest 145, 723–728 (2014).
pubmed: 24114524 doi: 10.1378/chest.13-1474
Kondoh, S. et al. Validation of the Japanese disease severity classification and the GAP model in Japanese patients with idiopathic pulmonary fibrosis. Respir. Investig. 54, 327–333 (2016).
pubmed: 27566380 doi: 10.1016/j.resinv.2016.02.009
Kreuter, M. et al. Monocyte count as a prognostic biomarker in patients with idiopathic pulmonary fibrosis. Am. J. Respir. Crit. Care Med. 204, 74–81 (2021).
pubmed: 33434107 pmcid: 8437112 doi: 10.1164/rccm.202003-0669OC
Maher, T. M. et al. Biomarkers of extracellular matrix turnover in patients with idiopathic pulmonary fibrosis given nintedanib (INMARK study): A randomised, placebo-controlled study. Lancet Respir. Med. 7, 771–779 (2019).
pubmed: 31326319 doi: 10.1016/S2213-2600(19)30255-3
Organ, L. A. et al. Biomarkers of collagen synthesis predict progression in the PROFILE idiopathic pulmonary fibrosis cohort. Respir. Res. 20, 148 (2019).
pubmed: 31299951 pmcid: 6624898 doi: 10.1186/s12931-019-1118-7
Rosas, I. O. et al. MMP1 and MMP7 as potential peripheral blood biomarkers in idiopathic pulmonary fibrosis. PLoS Med. 5, e93 (2008).
pubmed: 18447576 pmcid: 2346504 doi: 10.1371/journal.pmed.0050093
Prasse, A. et al. Serum CC-chemokine ligand 18 concentration predicts outcome in idiopathic pulmonary fibrosis. Am. J. Respir. Crit. Care Med. 179, 717–723 (2009).
pubmed: 19179488 doi: 10.1164/rccm.200808-1201OC
Neighbors, M. et al. Prognostic and predictive biomarkers for patients with idiopathic pulmonary fibrosis treated with pirfenidone: Post-hoc assessment of the CAPACITY and ASCEND trials. Lancet Respir. Med. 6, 615–626 (2018).
pubmed: 30072107 doi: 10.1016/S2213-2600(18)30185-1
Yokoyama, A. et al. Prognostic value of circulating KL-6 in idiopathic pulmonary fibrosis. Respirology 11, 164–168 (2006).
pubmed: 16548901 doi: 10.1111/j.1440-1843.2006.00834.x
Takahashi, H. et al. Serum surfactant proteins A and D as prognostic factors in idiopathic pulmonary fibrosis and their relationship to disease extent. Am. J. Respir. Crit. Care Med. 162, 1109–1114 (2000).
pubmed: 10988138 doi: 10.1164/ajrccm.162.3.9910080
Ishikawa, N., Hattori, N., Yokoyama, A. & Kohno, N. Utility of KL-6/MUC1 in the clinical management of interstitial lung diseases. Respir. Investig. 50, 3–13 (2012).
pubmed: 22554854 doi: 10.1016/j.resinv.2012.02.001
Conway, S. J. et al. The role of periostin in tissue remodeling across health and disease. Cell Mol. Life Sci. 71, 1279–1288 (2014).
pubmed: 24146092 doi: 10.1007/s00018-013-1494-y
Yamaguchi, Y. et al. Serum periostin levels are correlated with progressive skin sclerosis in patients with systemic sclerosis. Br. J. Dermatol. 168, 717–725 (2013).
pubmed: 23110679 doi: 10.1111/bjd.12117
Takayama, G. et al. Periostin: A novel component of subepithelial fibrosis of bronchial asthma downstream of IL-4 and IL-13 signals. J. Allergy Clin. Immunol. 118, 98–104 (2006).
pubmed: 16815144 doi: 10.1016/j.jaci.2006.02.046
Okamoto, M., Izuhara, K., Ohta, S., Ono, J. & Hoshino, T. Ability of periostin as a new biomarker of idiopathic pulmonary fibrosis. Adv. Exp. Med. Biol. 1132, 79–87 (2019).
pubmed: 31037627 doi: 10.1007/978-981-13-6657-4_9
Uchida, M. et al. Periostin, a matricellular protein, plays a role in the induction of chemokines in pulmonary fibrosis. Am. J. Respir. Cell Mol. Biol. 46, 677–686 (2012).
pubmed: 22246863 pmcid: 4304367 doi: 10.1165/rcmb.2011-0115OC
Okamoto, M. et al. Periostin, a matrix protein, is a novel biomarker for idiopathic interstitial pneumonias. Eur. Respir. J. 37, 1119–1127 (2011).
pubmed: 21177844 doi: 10.1183/09031936.00059810
Naik, P. K. et al. Periostin promotes fibrosis and predicts progression in patients with idiopathic pulmonary fibrosis. Am. J. Physiol .Lung Cell Mol. Physiol. 303, L1046-1056 (2012).
pubmed: 23043074 pmcid: 3532583 doi: 10.1152/ajplung.00139.2012
Tajiri, M. et al. Serum level of periostin can predict long-term outcome of idiopathic pulmonary fibrosis. Respir. Investig. 53, 73–81 (2015).
pubmed: 25745852 doi: 10.1016/j.resinv.2014.12.003
Ohta, S. et al. The usefulness of monomeric periostin as a biomarker for idiopathic pulmonary fibrosis. PLoS ONE 12, e0174547 (2017).
pubmed: 28355256 pmcid: 5371347 doi: 10.1371/journal.pone.0174547
Shimizu, H. et al. Association of serum monomeric periostin level with outcomes of acute exacerbation of idiopathic pulmonary fibrosis and fibrosing nonspecific interstitial pneumonia. Ann. Transl. Med. 9, 739 (2021).
pubmed: 34268352 pmcid: 8246219 doi: 10.21037/atm-21-414
Nukui, Y. et al. Periostin as a predictor of prognosis in chronic bird-related hypersensitivity pneumonitis. Allergol. Int. 68, 363–369 (2019).
pubmed: 30871804 doi: 10.1016/j.alit.2019.02.007
Collard, H. R. et al. Acute exacerbations of idiopathic pulmonary fibrosis. Am. J. Respir. Crit. Care Med. 176, 636–643 (2007).
pubmed: 17585107 doi: 10.1164/rccm.200703-463PP
Adegunsoye, A. et al. Circulating plasma biomarkers of survival in antifibrotic-treated patients with idiopathic pulmonary fibrosis. Chest 158, 1526–1534 (2020).
pubmed: 32450241 pmcid: 7545483 doi: 10.1016/j.chest.2020.04.066
Yoshikawa, T. et al. Surfactant protein A as a biomarker of outcomes of anti-fibrotic drug therapy in patients with idiopathic pulmonary fibrosis. BMC Pulm Med. 20, 27 (2020).
pubmed: 32005219 pmcid: 6995128 doi: 10.1186/s12890-020-1060-y
Inoue, Y. et al. Diagnostic and prognostic biomarkers for chronic fibrosing interstitial lung diseases with a progressive phenotype. Chest 158, 646–659 (2020).
pubmed: 32268131 doi: 10.1016/j.chest.2020.03.037
Lancaster, L. et al. Idiopathic pulmonary fibrosis: Physician and patient perspectives on the pathway to care from symptom recognition to diagnosis and disease burden. Respirology 27, 66–75 (2022).
pubmed: 34611971 doi: 10.1111/resp.14154
Salisbury, M. L. et al. Antifibrotic drug use in patients with idiopathic pulmonary fibrosis. Data from the IPF-PRO registry. Ann. Am. Thorac. Soc. 17, 1413–1423 (2020).
pubmed: 32574517 pmcid: 7640723 doi: 10.1513/AnnalsATS.201912-880OC
Karampitsakos, T., Juan-Guardela, B. M., Tzouvelekis, A. & Herazo-Maya, J. D. Precision medicine advances in idiopathic pulmonary fibrosis. EBioMedicine. 95, 104766 (2023).
pubmed: 37625268 pmcid: 10469771 doi: 10.1016/j.ebiom.2023.104766

Auteurs

Masaki Okamoto (M)

Division of Respirology, Neurology, and Rheumatology, Department of Internal Medicine, Kurume University School of Medicine, 67 Asahi-machi, Kurume, Fukuoka, 830-0011, Japan. okamoto_masaki@med.kurume-u.ac.jp.
Department of Respirology, NHO Kyushu Medical Center, 1-8-1 Jigyohama, Chuo-ku, Fukuoka, 810-0065, Japan. okamoto_masaki@med.kurume-u.ac.jp.

Kiminori Fujimoto (K)

Department of Radiology, Kurume University School of Medicine, 67 Asahi-machi, Kurume, Fukuoka, 830-0011, Japan.

Takeshi Johkoh (T)

Department of Radiology, Kansai Rosai Hospital, Inabasou 3-1-69, Amagasaki, Hyogo, 660-0064, Japan.

Atsushi Kawaguchi (A)

Education and Research Center for Community Medicine, Faculty of Medicine, Saga Medical School, 5-1-1 Nabeshima, Saga, 849-8501, Japan.

Hiroshi Mukae (H)

Department of Respiratory Medicine, Nagasaki University Graduate School of Biomedical Sciences, 1-7-1 Sakamoto, Nagasaki, 852-8501, Japan.

Noriho Sakamoto (N)

Department of Respiratory Medicine, Nagasaki University Graduate School of Biomedical Sciences, 1-7-1 Sakamoto, Nagasaki, 852-8501, Japan.

Takashi Ogura (T)

Division of Respiratory Medicine, Kanagawa Cardiovascular and Respiratory Center, 6-16-1 Tomiokahigashi, Yokohama, Kanagawa-ku, Kanagawa, 236-0051, Japan.

Satoshi Ikeda (S)

Division of Respiratory Medicine, Kanagawa Cardiovascular and Respiratory Center, 6-16-1 Tomiokahigashi, Yokohama, Kanagawa-ku, Kanagawa, 236-0051, Japan.

Yasuhiro Kondoh (Y)

Department of Respiratory Medicine and Allergy, Tosei General Hospital, 160 Nishioiwake, Seto, Aichi, 489-0065, Japan.

Yasuhiko Yamano (Y)

Department of Respiratory Medicine and Allergy, Tosei General Hospital, 160 Nishioiwake, Seto, Aichi, 489-0065, Japan.

Kosaku Komiya (K)

Respiratory Medicine and Infectious Diseases, Faculty of Medicine, Oita University, 1-1 Idaigaoka, Hasama-machi, Yufu, Oita, 879-5593, Japan.

Kenji Umeki (K)

Department of Respiratory Medicine, Tenshindo Hetsugi Hospital, 5956 Nakahetsugi, Oita, 879-7761, Japan.

Hirotaka Nishikiori (H)

Department of Respiratory Medicine and Allergology, Sapporo Medical University School of Medicine, South-1-West-16, Chuo-ku, Sapporo, Hokkaido, 060-8543, Japan.

Yoshinori Tanino (Y)

Department of Pulmonary Medicine, School of Medicine, Fukushima Medical University, 1 Hikarigaoka, Fukushima, Fukushima, 960-1295, Japan.

Toru Tsuda (T)

Kirigaoka Tsuda Hospital, 3-9-20 Kirigaoka, Kitakyushu, Fukuoka, 802-0052, Japan.

Naoki Arai (N)

Department of Respiratory Medicine, National Hospital Organization Ibarakihigashi National Hospital, 825 Terunuma, Tokai-mura, Ibaraki, 319-1113, Japan.

Masamichi Komatsu (M)

First Department of Internal Medicine, Shinshu University School of Medicine, 3-1-1 Asahi, Matsumoto, Nagano, 390-8621, Japan.

Susumu Sakamoto (S)

Department of Respiratory Medicine, Toho University Omori Medical Center, 6-11-1 Omorinishi, Tokyo, 143-8541, Japan.

Kazuhiro Yatera (K)

Department of Respiratory Medicine, University of Occupational and Environmental Health, 1-1 Iseigaoka, Kitakyushu, Fukuoka, 807-8555, Japan.

Yoshikazu Inoue (Y)

Clinical Research Center, National Hospital Organization Kinki-Chuo Chest Medical Center, 1180 Nagasone-cho, Sakai, Osaka, 591-8555, Japan.

Yasunari Miyazaki (Y)

Department of Respiratory Medicine, Graduate School of Medical and Dental Sciences, Tokyo Medical and Dental University, 1-5-45 Yushima, Tokyo, 113-8510, Japan.

Seishu Hashimoto (S)

Department of Respiratory Medicine, Tenri Hospital, 200 Mishima-cho, Tenri, Nara, 632-8552, Japan.

Yasuo Shimizu (Y)

Department of Pulmonary Medicine and Clinical Immunology, Dokkyo Medical University School of Medicine, 880 Kitakobayashi, Mibu, Shimotsuga, Tochigi, 321-0293, Japan.

Hironao Hozumi (H)

Second Division, Department of Internal Medicine, Hamamatsu University School of Medicine, 1-20-1 Handayama, Hamamatsu, Shizuoka, 431-3192, Japan.

Hiroshi Ohnishi (H)

Department of Respiratory Medicine and Allergology, Kochi Medical School, Kochi University, 185-1 Kohasu, Nankoku, Kochi, 783-8505, Japan.

Tomohiro Handa (T)

Department of Advanced Medicine for Respiratory Failure, Graduate School of Medicine, Kyoto University, 54 Shogoin Kawaharacho, Sakyo-ku, Kyoto, 606-8507, Japan.

Noboru Hattori (N)

Department of Molecular and Internal Medicine, Graduate School of Biomedical Sciences, Hiroshima University, 1-2-3 Kasumi, Minami-ku, Hiroshima, 734-8551, Japan.

Tomoo Kishaba (T)

Department of Respiratory Medicine, Okinawa Chubu Hospital, 281 Miyazato, Uruma, Okinawa, 904-2293, Japan.

Motoyasu Kato (M)

Department of Respiratory Medicine, Juntendo University Graduate School of Medicine, 2-1-1 Hongo, Tokyo, 113-8421, Japan.

Minoru Inomata (M)

Department of Respiratory Medicine, Japanese Red Cross Medical Center, 4-1-22 Hiroo, Tokyo, 150-8935, Japan.

Hiroshi Ishii (H)

Department of Respiratory Medicine, Fukuoka University Chikushi Hospital, 1-1-1 Zokumyouin, Chikushino, Fukuoka, 818-8502, Japan.

Naoki Hamada (N)

Department of Respiratory Medicine, Fukuoka University Hospital, 7-45-1 Nanakuma, Fukuoka, 814-0180, Japan.

Satoshi Konno (S)

Department of Respiratory Medicine, Faculty of Medicine, Hokkaido University, N15W7 Kita-ku, Sapporo, Hokkaido, 060-8638, Japan.

Yoshiaki Zaizen (Y)

Division of Respirology, Neurology, and Rheumatology, Department of Internal Medicine, Kurume University School of Medicine, 67 Asahi-machi, Kurume, Fukuoka, 830-0011, Japan.

Arata Azuma (A)

Respirology and Clinical Research Center, Mihara General Hospital and Nippon Medical School, Tokorozawa, Saitama, 359-0045, Japan.

Takafumi Suda (T)

Second Division, Department of Internal Medicine, Hamamatsu University School of Medicine, 1-20-1 Handayama, Hamamatsu, Shizuoka, 431-3192, Japan.

Kenji Izuhara (K)

Division of Medical Biochemistry, Department of Biomolecular Sciences, Saga Medical School, 5-1-1 Nabeshima, Saga, 849-8501, Japan.

Tomoaki Hoshino (T)

Division of Respirology, Neurology, and Rheumatology, Department of Internal Medicine, Kurume University School of Medicine, 67 Asahi-machi, Kurume, Fukuoka, 830-0011, Japan.

Classifications MeSH