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Nasal microbiota and symptom persistence in acute respiratory tract infections in infants

Roland P. Neumann, Markus Hilty, Binbin Xu, Jakob Usemann, Insa Korten, Moana Mika, Loretta Müller, Philipp Latzin, Urs Frey
ERJ Open Research 2018 4: 00066-2018; DOI: 10.1183/23120541.00066-2018
Roland P. Neumann
University Children's Hospital Basel UKBB, University of Basel, Basel, SwitzerlandBoth authors contributed equally
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Markus Hilty
Institute for Infectious Diseases, University of Bern, Bern, SwitzerlandDept of Infectious Diseases, Bern University Hospital, Bern, SwitzerlandBoth authors contributed equally
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Binbin Xu
University Children's Hospital Basel UKBB, University of Basel, Basel, Switzerland
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Jakob Usemann
University Children's Hospital Basel UKBB, University of Basel, Basel, SwitzerlandPediatric Respiratory Medicine, Dept of Pediatrics, Inselspital, Bern University Hospital, University of Bern, Bern, Switzerland
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  • ORCID record for Jakob Usemann
Insa Korten
University Children's Hospital Basel UKBB, University of Basel, Basel, SwitzerlandPediatric Respiratory Medicine, Dept of Pediatrics, Inselspital, Bern University Hospital, University of Bern, Bern, Switzerland
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Moana Mika
Institute for Infectious Diseases, University of Bern, Bern, SwitzerlandGraduate School for Cellular and Biomedical Sciences, University of Bern, Bern, Switzerland
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Loretta Müller
University Children's Hospital Basel UKBB, University of Basel, Basel, Switzerland
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Philipp Latzin
Pediatric Respiratory Medicine, Dept of Pediatrics, Inselspital, Bern University Hospital, University of Bern, Bern, Switzerland
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Urs Frey
University Children's Hospital Basel UKBB, University of Basel, Basel, Switzerland
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  • For correspondence: urs.frey@ukbb.ch
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  • FIGURE 1
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    FIGURE 1

    Flow chart of the study population. ARI: acute respiratory tract infection.

  • FIGURE 2
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    FIGURE 2

    Composition of the most common clusters at the a) onset of the first acute respiratory tract infection (swab A) and b) 3 weeks later (swab B) illustrated as bacterial abundances of the five most common bacterial families with the remaining grouped as “Others”. Clusters with sizes of <5% are not depicted.

  • FIGURE 3
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    FIGURE 3

    Results of hierarchical clustering based on the microbial composition at the onset of the first acute respiratory tract infection (swab A) and 3 weeks later (swab B). The size of the circles and the numbers inside indicate the number of individuals assigned to each cluster. The connecting bars indicate the transition from one particular cluster to another between swabs A and B; the size of the bars corresponds to the number of transitioning individuals. The dominating bacterial families in the clusters are as follows. A1: Moraxellaceae; A2: Moraxellaceae and Streptococcaeae; A3: Streptococcaceae; A4: “Others”; A5: Pasteurellaceae; B1: Moraxellaceae; B2: “Others”; B3: Streptococcaceae. Areas in the circles of darker green on the left side of the panel indicate the proportion of infants at swab A in each cluster who were asymptomatic at swab B compared to the proportion of symptomatic infants at swab B (lighter green). Areas in the circles of darker orange on the right side of the panel indicate the proportion of asymptomatic infants at swab B compared to the proportion of symptomatic infants (lighter orange). SDI: Shannon Diversity Index, presented as the median value.

Tables

  • Figures
  • Supplementary Materials
  • TABLE 1

    Baseline characteristics of the study population

    Total participants n (% male)167 (57)
    Mean±sd gestational age weeks39.3±2.0
    Mean±sd birth weight kg3.3±0.55
    Caesarean section25 (15)
    Season of birth
     Spring62 (37)
     Summer44 (26)
     Autumn32 (19)
     Winter29 (17)
    Mean±sd (range) age at ARI weeks29.9±12.5 (2–52)
    Season at first ARI
     Spring40 (24)
     Summer14 (8)
     Autumn38 (23)
     Winter75 (45)
    Increased atopy risk109 (65)
    Childcare attendance32 (19)
    Breastfeeding status at time of ARI#99 (60)
    Environmental tobacco smoke exposure24 (14)
    Other siblings (living in the same household)106 (63)
     One sibling75 (45)
     ≥2 siblings31 (19)

    Data are presented as n (%), unless otherwise stated. ARI: acute respiratory tract infection. #: infants being breastfed at the time of ARI.

    • TABLE 2

      Abundances of bacterial families and alpha diversity measurements at the onset of the acute respiratory tract infection (ARI) and 3 weeks after the onset

      At ARI onset (swab A)3 weeks after ARI onset (swab B)
      Bacterial family abundance %
       Moraxellaceae52.4 (66.5)49.5 (66.2)
       Streptococcaceae19.2 (41.03)16.31 (33.9)
       Corynebacteriaceae0.1 (0.7)0.2 (1.1)#
       Pasteurellaceae0.4 (1.9)0.3 (1.5)
       Staphylococcaceae0.1 (0.6)0.1 (0.6)
        “Others”6.6 (14.7)9.4 (27.3)#
      Alpha diversity measurements
       SDI1.0 (0.8)1.1 (1.2)¶
       Bacterial richness33 (35)38 (36)¶

      Data are presented as median (interquartile range). SDI: Shannon Diversity Index. #: abundance of Corynebacteriaceae and “Others” were significantly different between swab A and swab B (p=0.002 and 0.004, respectively, Wilcoxon signed rank sum test); ¶: SDI and bacterial richness are lower at swab A compared to swab B (p=0.013 and 0.052, respectively, Wilcoxon signed rank sum test).

      • TABLE 3

        Infant clusters at the onset of acute respiratory tract infection (swab A) and subsequent presence of symptoms

        Cluster (n=165)p-value
        A1 (n=56)A2 (n=51)A3 (n=31)A4 (n=14)A5 (n=13)
        Symptomatic after 1 week38 (67.8)43 (84.3) ↑19 (61.3)8 (53.3)9 (69.2)0.121#
        Symptomatic after 2 weeks17 (30.4)19 (37.3) ↑4 (12.9) ↓1 (7.1) ↓4 (30.8)0.061¶
        Symptomatic after 3 weeks19 (33.9)12 (23.5)8 (25.8)4 (28.6)5 (38.5)0.754¶
        Continuously symptomatic for ≥3 weeks13 (23.3)9 (17.6)2 (6.5) ↓1 (7.1)3 (23.1)0.329¶

        Data are presented as n (%), unless otherwise stated. Statistical analyses were performed using #: Chi-squared; or ¶: Fisher's exact test. Significant overrepresentation (↑) and significant underrepresentation (↓) of presence of symptoms in the clusters was assessed by enrichment analysis. The dominating bacterial families in the clusters are as follows. A1: Moraxellaceae; A2: Moraxellaceae and Streptococcaeae; A3: Streptococcaceae; A4: “Others”; A5: Pasteurellaceae.

        • TABLE 4

          Infant clusters 3 weeks after onset of acute respiratory tract infection (ARI) (swab B) and subsequent presence of symptoms after the onset of the first ARI

          Cluster (n=155)B1 (n=96)B2 (n=34)B3 (n=25)p-value
          Symptomatic after 1 week70 (72.9)22 (64.7)16 (64.0)0.135#
          Symptomatic after 2 weeks28 (30.2)5 (14.7) ↓9 (36.0)0.454#
          Symptomatic after 3 weeks27 (29.2)2 (5.9) ↓14 (56.0) ↑<0.001¶
          Continuously symptomatic for ≥3 weeks16 (16.7)1 (2.9) ↓9 (36.0) ↑0.010¶

          Data are presented as n (%), unless otherwise stated. Statistical analyses were performed using #: Chi-squared; or ¶: Fisher's exact test. Significant overrepresentation (↑) and significant underrepresentation (↓) of presence of symptoms in the clusters was assessed by enrichment analysis. The dominating bacterial families in the clusters are as follows. B1: Moraxellaceae; B2: “Others”; B3: Streptococcaceae.

          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.

            Supplementary methods 00066-2018_Supplementary_methods

            Supplementary table S1 00066-2018_Table_S1

            Supplementary table S2 00066-2018_Table_S2

            Supplementary table S3 00066-2018_Table_S3

            Supplementary table S4 00066-2018_Table_S4

            Supplementary table S5 00066-2018_Table_S5

            Supplementary table S6 00066-2018_Table_S6

            Supplementary table S7 00066-2018_Table_S7

            Supplementary table S8 00066-2018_Table_S8

            Supplementary table S9 00066-2018_Table_S9

            Supplementary table S10 00066-2018_Table_S10

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          Nasal microbiota and symptom persistence in acute respiratory tract infections in infants
          Roland P. Neumann, Markus Hilty, Binbin Xu, Jakob Usemann, Insa Korten, Moana Mika, Loretta Müller, Philipp Latzin, Urs Frey
          ERJ Open Research Oct 2018, 4 (4) 00066-2018; DOI: 10.1183/23120541.00066-2018

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          Nasal microbiota and symptom persistence in acute respiratory tract infections in infants
          Roland P. Neumann, Markus Hilty, Binbin Xu, Jakob Usemann, Insa Korten, Moana Mika, Loretta Müller, Philipp Latzin, Urs Frey
          ERJ Open Research Oct 2018, 4 (4) 00066-2018; DOI: 10.1183/23120541.00066-2018
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