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Prognostic impact of pre-existing interstitial lung disease in non-HIV patients with Pneumocystis pneumonia

Shohei Hamada, Hidenori Ichiyasu, Megumi Inaba, Hiroshi Takahashi, Tomoki Sadamatsu, Kimitaka Akaike, Aiko Masunaga, Yasumasa Tashiro, Naomi Hirata, Takeshi Yoshinaga, Takuro Sakagami
ERJ Open Research 2020 6: 00306-2019; DOI: 10.1183/23120541.00306-2019
Shohei Hamada
1Dept of Respiratory Medicine, Kumamoto University Hospital, Faculty of Life Sciences, Kumamoto University, Kumamoto, Japan
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Hidenori Ichiyasu
1Dept of Respiratory Medicine, Kumamoto University Hospital, Faculty of Life Sciences, Kumamoto University, Kumamoto, Japan
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  • For correspondence: ichiyasu@kumamoto-u.ac.jp
Megumi Inaba
2Division of Respiratory Medicine, Kumamoto Chuo Hospital, Kumamoto, Japan
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Hiroshi Takahashi
1Dept of Respiratory Medicine, Kumamoto University Hospital, Faculty of Life Sciences, Kumamoto University, Kumamoto, Japan
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Tomoki Sadamatsu
3Dept of Respiratory Medicine, Minamata City General Hospital and Medical Center, Minamata, Japan
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Kimitaka Akaike
1Dept of Respiratory Medicine, Kumamoto University Hospital, Faculty of Life Sciences, Kumamoto University, Kumamoto, Japan
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Aiko Masunaga
1Dept of Respiratory Medicine, Kumamoto University Hospital, Faculty of Life Sciences, Kumamoto University, Kumamoto, Japan
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Yasumasa Tashiro
3Dept of Respiratory Medicine, Minamata City General Hospital and Medical Center, Minamata, Japan
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Naomi Hirata
2Division of Respiratory Medicine, Kumamoto Chuo Hospital, Kumamoto, Japan
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Takeshi Yoshinaga
2Division of Respiratory Medicine, Kumamoto Chuo Hospital, Kumamoto, Japan
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Takuro Sakagami
1Dept of Respiratory Medicine, Kumamoto University Hospital, Faculty of Life Sciences, Kumamoto University, Kumamoto, Japan
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  • FIGURE 1
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    FIGURE 1

    Inclusion and exclusion flow diagram. PCP: Pneumocystis pneumonia; GMS: Gomori methenamine silver; ILD: interstitial lung disease.

  • FIGURE 2
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    FIGURE 2

    Kaplan–Meier comparison of survival curves between the interstitial lung disease (ILD) and non-ILD groups. The 90-day mortality was significantly higher in the ILD group than in the non-ILD group (62.5% versus 19.0%). PCP: Pneumocystis pneumonia.

  • FIGURE 3
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    FIGURE 3

    Kaplan–Meier comparison of survival curves between lower and higher percentage of bronchoalveolar lavage fluid (BALF) neutrophil groups. The patients were categorised into the “higher” or “lower” group according to the median percentage of BALF neutrophils. a) With regards to all subjects as a whole, the 90-day survival was significantly worse in the higher group (n=28) than in the lower group (n=23) (90-day mortality rate in the higher group: 50.0%; lower group: 17.4%). b) In the interstitial lung disease (ILD) group, the 90-day survival was significantly worse in the higher group (n=12) than in the lower group (n=10) (higher group: 90.0%; lower group: 50.0%). c) In the non-ILD group, the 90-day survival was not different between the higher group (n=14) and the lower group (n=15) (higher group: 13.3%; lower group: 7.1%).

  • FIGURE 4
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    FIGURE 4

    Comparisons of serum levels of β-d-glucan and Krebs von den Lungen-6 (KL-6) before and after Pneumocystis pneumonia treatment. The levels of β-d-glucan significantly decreased in both groups: a) median value of the interstitial lung disease (ILD) group from 78.5 to 38.5 pg·mL−1, p=0.006; b) non-ILD group from 95.0 to 27.0 pg·mL−1, p=0.001). c) The level of KL-6 significantly increased in the ILD group (median value from 1505.0 to 2730.0 U·mL−1, p=0.001) and d) did not change significantly in the non-ILD group (median value from 659.5 to 550.0 U·mL−1, p=0.249).

  • FIGURE 5
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    FIGURE 5

    Kaplan–Meier comparison of survival curves in the interstitial lung disease patients divided by increasing or decreasing Krebs von den Lungen-6 (KL-6) levels after Pneumocystis pneumonia (PCP) treatment. The 90-day mortality of the patients with increasing KL-6 after the treatment was significantly higher than those with decreasing KL-6 (increasing KL-6, n=19: 78.9%; decreasing KL-6, n=5: 0%).

Tables

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  • TABLE 1

    Patient characteristics

    AllILD groupnon-ILD groupp-value
    Subjects743242
    Age years73.5 (66.0–80.0)74.0 (68.5–80.8)68.0 (66.5–73.0)0.125
    Male sex40 (83.3%)22 (68.8%)27 (64.3%)0.805
    Ever-smokers46 (62.2%)20 (62.5%)26 (61.9%)1.000
    BMI kg·m−221.8 (19.5–24.0)22.4 (19.1–24.0)21.0 (19.8–24.0)0.291
    Previous use of corticosteroids69 (93.2%)31 (96.9%)38 (90.5%)0.381
    Previous use of immunosuppressants27 (36.5%)10 (31.3%)17 (40.5%)0.471
    PCP prophylaxis1 (1.4%)0 (0.0%)1 (2.4%)1.000
    Underlying diseases
     IIPs9 (12.2%)9 (28.1%)0 (0.0%)<0.001
     CTD24 (32.4%)11 (34.4%)13 (31.0%)0.806
     Solid tumour20 (27.0%)5 (15.6%)15 (35.7%)0.067
     Haematologic malignancy8 (10.8%)2 (6.3%)6 (14.3%)0.453
     Others13 (17.6%)5 (15.6%)8 (19.0%)0.331
    Diagnostic procedures of PCP
     BALF GMS stain19 (25.7%)11 (34.4%)8 (19.0%)0.181
     BALF PCR38 (51.4%)15 (46.9%)23 (54.8%)0.639
     Sputum PCR23 (31.1%)9 (28.1%)14 (33.3%)0.800
    Laboratory findings
     Lymphocyte count cells per µL695.0 (346.0–1067.5)648.0 (326.0–980.0)695.0 (367.0–1100.0)0.688
     Albumin mg·dL−12.7 (2.3–3.1)2.6 (2.4–2.9)2.8 (2.2–3.4)0.271
     LDH U·L−1434.0 (295.0–540.5)434.0 (298.0–544.0)453.0 (293.0–544.0)0.819
     KL-6# U·mL−1754.0 (476.0–1705.0)1170.0 (703.0–2271.8)585.5 (411.5–965.8)0.001
     CRP mg·dL−16.7 (3.3–11.5)4.8 (2.1–10.9)6.9 (5.0–14.0)0.230
     eGFR mL·min−1·1.73 m−260.2 (42.3–81.5)58.0 (43.0–69.9)64.7 (41.8–85.1)0.285
     β-d-glucan pg·mL−187.0 (66.0–80.0)78.4 (28.5–281.8)86.7 (46.8–240.0)0.382
    PaO2/FIO2 ratio248.0 (155.8–298.0)175.0 (107.0–289.5)251.5 (180.0–301.0)0.025
    BALF findings¶
     Neutrophils12.2% (4.9–40.5%)22.6% (10.6–47.9%)6.6% (3.2–38.1%)0.012
     Lymphocytes34.3% (11.3–55.3%)30.0% (9.5–48.0%)46.0% (8.75–64.9%)0.101
     Eosinophils1.0% (0.0–2.3%)0.2% (0.0–2.0%)1.0% (0.0–3.0%)0.69
     Macrophages34.0% (18.0–49.0%)37.5% (22.3–54.8%)33.0% (18.0–49.0%)0.312

    Data are presented as median (interquartile range) unless otherwise stated. ILD: interstitial lung disease; BMI: body mass index; PCP: Pneumocystis pneumonia; IIP: idiopathic interstitial pneumonia; CTD: connective tissue disease; BALF: bronchoalveolar lavage fluid; GMS: Gomori methenamine silver; LDH: lactate dehydrogenase; KL-6: Krebs von den Lungen-6; CRP: C-reactive protein; eGFR: estimated glomerular filtration rate; PaO2: arterial oxygen tension; FIO2: inspiratory oxygen fraction. #: n=69; ¶: n=53. The p-values refer to comparisons between the ILD and non-ILD groups.

    • TABLE 2

      Clinical diagnosis and high-resolution computed tomography (HRCT) patterns of interstitial lung disease (ILD)

      Patients#
      Clinical diagnosis of ILD
       IIPs17 (53.1%)
        IPF8 (25.0%)
        Non-IPF9 (28.1%)
       Non-IIPs15 (46.9%)
        CTD-ILD11 (34.4%)
        CHP1 (3.1%)
        CEP1 (3.1%)
        Asbestosis1 (3.1%)
        Radiation pneumonitis1 (3.1%)
      HRCT patterns of ILD
       UIP pattern11 (34.4%)
       Non-UIP pattern21 (65.6%)

      IIP: idiopathic interstitial pneumonia; IPF: idiopathic pulmonary fibrosis; CTD: connective tissue disease; CHP: chronic hypersensitivity pneumonia; CEP: chronic eosinophilic pneumonia; UIP: usual interstitial pneumonia. #: n=32.

      • TABLE 3

        Univariate and multivariate analyses of predictors of 90-day mortality

        VariablesHR (95% CI)p-value
        Univariate analysis
         Pre-existing ILD4.003 (1.761–9.098)0.001
         Steroid pulse therapy3.135 (1.488–6.606)0.004
         Albumin0.364 (0.214–0.621)<0.001
         KL-61.000 (1.000–1.001)0.002
         LDH1.002 (1.000–1.003)0.074
         CRP1.045 (0.992–1.101)0.095
          PaO2/FIO2 ratio0.991 (0.987–0.996)<0.001
        Multivariate analysis
         Pre-existing ILD5.952 (1.900–18.649)0.002
         Albumin0.312 (0.131–0.743)0.009

        HR: hazard ratio; ILD: interstitial lung disease; KL-6: Krebs von den Lungen-6; LDH: lactate dehydrogenase; CRP: C-reactive protein; PaO2: arterial oxygen tension; FIO2: inspiratory oxygen fraction.

        Supplementary Materials

        • Figures
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        • Supplementary Material

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

          Table S1 00306-2019.SUPPLEMENT

          Figure S1 00306-2019.figureS1

          Figure S2 00306-2019.figureS2

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        Prognostic impact of pre-existing interstitial lung disease in non-HIV patients with Pneumocystis pneumonia
        Shohei Hamada, Hidenori Ichiyasu, Megumi Inaba, Hiroshi Takahashi, Tomoki Sadamatsu, Kimitaka Akaike, Aiko Masunaga, Yasumasa Tashiro, Naomi Hirata, Takeshi Yoshinaga, Takuro Sakagami
        ERJ Open Research Apr 2020, 6 (2) 00306-2019; DOI: 10.1183/23120541.00306-2019

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        Prognostic impact of pre-existing interstitial lung disease in non-HIV patients with Pneumocystis pneumonia
        Shohei Hamada, Hidenori Ichiyasu, Megumi Inaba, Hiroshi Takahashi, Tomoki Sadamatsu, Kimitaka Akaike, Aiko Masunaga, Yasumasa Tashiro, Naomi Hirata, Takeshi Yoshinaga, Takuro Sakagami
        ERJ Open Research Apr 2020, 6 (2) 00306-2019; DOI: 10.1183/23120541.00306-2019
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