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Validation of a new serum granulocyte–macrophage colony-stimulating factor autoantibody testing kit

Koh Nakata, Tatsuki Sugi, Keiko Kuroda, Kazutaka Yoshizawa, Toshinori Takada, Ryushi Tazawa, Takahiro Ueda, Ami Aoki, Mitsuhiro Abe, Koichiro Tatsumi, Ryosuke Eda, Shotaro Kondoh, Konosuke Morimoto, Takeshi Tanaka, Etsuro Yamaguchi, Ayumu Takahashi, Miku Oda, Haruyuki Ishii, Shinyu Izumi, Haruhito Sugiyama, Atsushi Nakagawa, Keisuke Tomii, Masaru Suzuki, Satoshi Konno, Shinya Ohkouchi, Taizou Hirano, Tomohiro Handa, Toyohiro Hirai, Yoshikazu Inoue, Toru Arai, Katsuaki Asakawa, Takuro Sakagami, Takahiro Tanaka, Ayako Mikami, Nobutaka Kitamura
ERJ Open Research 2020 6: 00259-2019; DOI: 10.1183/23120541.00259-2019
Koh Nakata
1Clinical and Translational Research Center, Niigata University Medical and Dental Hospital, Niigata, Japan
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  • For correspondence: radical@med.niigata-u.ac.jp
Tatsuki Sugi
2IVD Development Unit, Ina Laboratory, Medical and Biological Laboratories, Ltd, Nagoya, Japan
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Keiko Kuroda
2IVD Development Unit, Ina Laboratory, Medical and Biological Laboratories, Ltd, Nagoya, Japan
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Kazutaka Yoshizawa
3Dept of Respiratory and Infectious Disease, Niigata University Medical and Dental Hospital, Niigata, Japan
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Toshinori Takada
4Uonuma Institute of Community Medicine, Niigata University Medical and Dental Hospital, Minami-Uonuma, Japan
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  • ORCID record for Toshinori Takada
Ryushi Tazawa
5Health Administration Center, Tokyo Medical and Dental University, Tokyo, Japan
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Takahiro Ueda
6Office of New Drug IV, Pharmaceuticals and Medical Devices Agency, Tokyo, Japan
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Ami Aoki
3Dept of Respiratory and Infectious Disease, Niigata University Medical and Dental Hospital, Niigata, Japan
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Mitsuhiro Abe
7Dept of Respirology, Graduate School of Medicine, Chiba University, Chiba, Japan
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Koichiro Tatsumi
7Dept of Respirology, Graduate School of Medicine, Chiba University, Chiba, Japan
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Ryosuke Eda
8Kurashiki Municipal Hospital, Kurashiki, Japan
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Shotaro Kondoh
8Kurashiki Municipal Hospital, Kurashiki, Japan
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Konosuke Morimoto
9Dept of Clinical Medicine, Institute of Tropical Medicine, Nagasaki University, Nagasaki, Japan
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Takeshi Tanaka
9Dept of Clinical Medicine, Institute of Tropical Medicine, Nagasaki University, Nagasaki, Japan
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Etsuro Yamaguchi
10Division of Respiratory Medicine and Allergology, Dept of Medicine, Aichi Medical University School of Medicine, Aichi, Japan
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Ayumu Takahashi
10Division of Respiratory Medicine and Allergology, Dept of Medicine, Aichi Medical University School of Medicine, Aichi, Japan
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Miku Oda
11Dept of Respiratory Medicine, Kyorin University School of Medicine, Tokyo, Japan
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Haruyuki Ishii
11Dept of Respiratory Medicine, Kyorin University School of Medicine, Tokyo, Japan
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Shinyu Izumi
12Dept of Respiratory Medicine, Center Hospital of the National Center for Global Health and Medicine, Tokyo, Japan
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Haruhito Sugiyama
12Dept of Respiratory Medicine, Center Hospital of the National Center for Global Health and Medicine, Tokyo, Japan
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Atsushi Nakagawa
13Kobe City Medical Center General Hospital, Kobe, Japan
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Keisuke Tomii
13Kobe City Medical Center General Hospital, Kobe, Japan
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Masaru Suzuki
14Dept of Respiratory Medicine, Faculty of Medicine and Graduate School of Medicine, Hokkaido University, Sapporo, Japan
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  • ORCID record for Masaru Suzuki
Satoshi Konno
14Dept of Respiratory Medicine, Faculty of Medicine and Graduate School of Medicine, Hokkaido University, Sapporo, Japan
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Shinya Ohkouchi
15Dept of Respiratory Medicine and Dept of Occupational Health, Tohoku University Graduate School of Medicine, Sendai, Japan
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Taizou Hirano
15Dept of Respiratory Medicine and Dept of Occupational Health, Tohoku University Graduate School of Medicine, Sendai, Japan
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Tomohiro Handa
16Dept of Advanced Medicine for Respiratory Failure and Department of Respiratory Medicine, Graduate School of Medicine, Kyoto University, Kyoto, Japan
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Toyohiro Hirai
16Dept of Advanced Medicine for Respiratory Failure and Department of Respiratory Medicine, Graduate School of Medicine, Kyoto University, Kyoto, Japan
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Yoshikazu Inoue
17National Hospital Organization Kinki-Chuo Chest Medical Center, Osaka, Japan
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Toru Arai
17National Hospital Organization Kinki-Chuo Chest Medical Center, Osaka, Japan
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Katsuaki Asakawa
3Dept of Respiratory and Infectious Disease, Niigata University Medical and Dental Hospital, Niigata, Japan
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Takuro Sakagami
18Dept of Respiratory Medicine, Kumamoto University Hospital, Kumamoto, Japan
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Takahiro Tanaka
1Clinical and Translational Research Center, Niigata University Medical and Dental Hospital, Niigata, Japan
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Ayako Mikami
12Dept of Respiratory Medicine, Center Hospital of the National Center for Global Health and Medicine, Tokyo, Japan
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Nobutaka Kitamura
1Clinical and Translational Research Center, Niigata University Medical and Dental Hospital, Niigata, Japan
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  • Article
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Figures

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  • FIGURE 1
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    FIGURE 1

    Distribution of the concentration of granulocyte–macrophage colony-stimulating factor autoantibody (GMAb) in serum samples in the training study. a) A bee swarm plot of the serum GMAb concentrations in 78 patients with autoimmune pulmonary alveolar proteinosis (aPAP) and 90 healthy controls (HC) measured using the newly developed GMAb measuring kit (MBL2490023). b) A histogram of logarithmic serum concentrations in the same patients and healthy subjects as shown in (a).

  • FIGURE 2
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    FIGURE 2

    Comparison of the performance of ELISA between the newly developed kit and the conventional method. Granulocyte–macrophage colony-stimulating factor autoantibody (GMAb) concentrations measured a) by the modified conventional ELISA kit or b) by the newly developed ELISA kit in the sera from 90 healthy subjects that were previously incubated with or without excess recombinant granulocyte–macrophage colony-stimulating factor (GM-CSF) (50 mg·mL−1). c) The correlation coefficient of the concentrations between the newly developed and the conventional methods was 0.80 in the healthy subjects and 0.95 in the patients with autoimmune pulmonary alveolar proteinosis. d) Receiver operating characteristic curve analysis (area under the curve 1.0).

  • FIGURE 3
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    FIGURE 3

    Estimation of the cut-off value between the healthy subjects and the patients using the logistic regression methods.

  • FIGURE 4
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    FIGURE 4

    Verification of the cut-off value (1.65 U·mL−1) using data obtained from the sera of patients with autoimmune (aPAP) (n=213), secondary (sPAP) (n=40) and hereditary pulmonary alveolar proteinosis (hPAP) (n=5), and other lung diseases (h=162). GMAb: granulocyte–macrophage colony-stimulating factor autoantibody.

  • FIGURE 5
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    FIGURE 5

    Exclusive plots for a) granulocyte–macrophage colony-stimulating factor autoantibody (GMAb) versus anti-melanoma differentiation-associated protein (MDA)-5 antibody (Ab), b) GMAb versus anti-aminoacyl transfer RNA synthetase (ARS) Ab and c) anti-MDA-5 Ab versus anti-ARS Ab. Red: autoimmune pulmonary alveolar proteinosis; blue: other patients.

Tables

  • Figures
  • Supplementary Materials
  • TABLE 1

    Demographic data of subjects in the training study

    CharacteristicsHealthy subjectsaPAP patients
    Subjects n9078
    Male/female n37/5332/46
    Age years mean±sd56.4±14.158.7±12.3
    Asian/Caucasian n22/6878/0
    Serum GMAb concentration U·mL−1
     Mean±sd0.151±0.10990.95±123.0
     Maximum0.71718.7
     Minimum0.0182.59

    aPAP: autoimmune pulmonary alveolar proteinosis; GMAb: granulocyte–macrophage colony-stimulating factor autoantibody.

    • TABLE 2

      Demographic data of cases in the validation study

      CharacteristicsaPAPsPAPhPAPOther lung diseases
      Subjects n213405162
      Male/female n122/6019/210/586/75
      Age years mean±sd52.6±14.757.6±13.356.4±14.566.2±12.0
      Asian/Caucasian n213/040/05/0162/0
      Serum GMAb concentration U·mL−1
       Mean±sd103.6±127.50.191±0.3020.148±0.1410.517±.818
       Maximum899.91.90.3848.57
       Minimum5.590.040.020.01
      Diagnostic procedures n
       BAL213365144
       VATS04017
       Autopsy0001
      Other lung diseases n
       CTD45
       DIPD20
       IIPs60
        IPF8
        Other IIPs52
       Infectious disease19
       Miscellaneous18

      Connective tissue disease (CTD) cases included five amyopathic dermatomyositis cases, 11 polymyositis/dermatomyositis interstitial lung diseases, 11 rheumatoid arthritis cases, four Sjögren syndromes, five systemic scleroses and nine other diseases. Infectious disease cases included eight Pneumocystis pneumonias, four bacterial pneumonias, three influenza pneumonias and four other infectious diseases. Miscellaneous diseases included four alveolar haemorrhages, three chronic eosinophilic pneumonias, two acute respiratory distress syndromes, two chronic hypersensitivity pneumonias and seven other diseases. aPAP: autoimmune pulmonary alveolar proteinosis; sPAP: secondary pulmonary alveolar proteinosis; hPAP: hereditary pulmonary alveolar proteinosis; GMAb: granulocyte–macrophage colony-stimulating factor autoantibody; BAL: bronchoalveolar lavage; VATS: video-assisted thoracic surgery; DIPD: drug-induced pulmonary disease; IIP: idiopathic interstitial pneumonia; IPF: idiopathic pulmonary fibrosis.

      • TABLE 3

        Demographic characteristics of patients with granulocyte–macrophage colony-stimulating factor autoantibody (GMAb) >1.65 U·mL−1

        CaseAge yearsSexDiagnosisGMAb U·mL−1Anti-MDA-5 AbAnti-ARS Ab
        163MsPAP (MDS)1.90NegativeNegative
        276FIIPs2.56NegativeNegative
        375MCTD48.57NegativeNegative
        468MCTD2.85NegativeNegative
        573FIIPs2.85NegativeNegative

        MDA: melanoma differentiation-associated protein; Ab: antibody; ARS: aminoacyl transfer RNA synthetase; M: male; F: female; sPAP: secondary pulmonary alveolar proteinosis; MDS: myelodysplastic syndrome; IIP: idiopathic interstitial pneumonia; CTD: connective tissue disease.

        Supplementary Materials

        • Figures
        • Tables
        • Supplementary Material

          Please note: supplementary material is not edited by the Editorial Office, and is uploaded as it has been supplied by the author.

          Supplementary material 00259-2019.supp

          Figure S1 00259-2019.figureS1

          Figure S2 00259-2019.figureS2

          Figure S3 00259-2019.figureS3

          Figure S4 00259-2019.figureS4

          Figure S5 00259-2019.figureS5

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        Validation of a new serum granulocyte–macrophage colony-stimulating factor autoantibody testing kit
        Koh Nakata, Tatsuki Sugi, Keiko Kuroda, Kazutaka Yoshizawa, Toshinori Takada, Ryushi Tazawa, Takahiro Ueda, Ami Aoki, Mitsuhiro Abe, Koichiro Tatsumi, Ryosuke Eda, Shotaro Kondoh, Konosuke Morimoto, Takeshi Tanaka, Etsuro Yamaguchi, Ayumu Takahashi, Miku Oda, Haruyuki Ishii, Shinyu Izumi, Haruhito Sugiyama, Atsushi Nakagawa, Keisuke Tomii, Masaru Suzuki, Satoshi Konno, Shinya Ohkouchi, Taizou Hirano, Tomohiro Handa, Toyohiro Hirai, Yoshikazu Inoue, Toru Arai, Katsuaki Asakawa, Takuro Sakagami, Takahiro Tanaka, Ayako Mikami, Nobutaka Kitamura
        ERJ Open Research Jan 2020, 6 (1) 00259-2019; DOI: 10.1183/23120541.00259-2019

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        Validation of a new serum granulocyte–macrophage colony-stimulating factor autoantibody testing kit
        Koh Nakata, Tatsuki Sugi, Keiko Kuroda, Kazutaka Yoshizawa, Toshinori Takada, Ryushi Tazawa, Takahiro Ueda, Ami Aoki, Mitsuhiro Abe, Koichiro Tatsumi, Ryosuke Eda, Shotaro Kondoh, Konosuke Morimoto, Takeshi Tanaka, Etsuro Yamaguchi, Ayumu Takahashi, Miku Oda, Haruyuki Ishii, Shinyu Izumi, Haruhito Sugiyama, Atsushi Nakagawa, Keisuke Tomii, Masaru Suzuki, Satoshi Konno, Shinya Ohkouchi, Taizou Hirano, Tomohiro Handa, Toyohiro Hirai, Yoshikazu Inoue, Toru Arai, Katsuaki Asakawa, Takuro Sakagami, Takahiro Tanaka, Ayako Mikami, Nobutaka Kitamura
        ERJ Open Research Jan 2020, 6 (1) 00259-2019; DOI: 10.1183/23120541.00259-2019
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