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Lung ultrasound patterns in paediatric pneumonia in Mozambique and Pakistan

Amy Sarah Ginsburg, Pio Vitorino, Zunera Qasim, Jennifer L. Lenahan, Jun Hwang, Alessandro Lamorte, Marta Valente, Benazir Balouch, Carmen Muñoz Almagro, M. Imran Nisar, Susanne May, Fyezah Jehan, Quique Bassat, Giovanni Volpicelli
ERJ Open Research 2021 7: 00518-2020; DOI: 10.1183/23120541.00518-2020
Amy Sarah Ginsburg
1Dept of Biostatistics, University of Washington, Seattle, WA, USA
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  • For correspondence: messageforamy@gmail.com
Pio Vitorino
2Centro de Investigação em Saúde de Manhiça (CISM), Maputo, Mozambique
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Zunera Qasim
3Dept of Pediatrics and Child Health, Aga Khan University, Karachi, Pakistan
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Jennifer L. Lenahan
4Save the Children Federation, Inc., Seattle, WA, USA
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Jun Hwang
1Dept of Biostatistics, University of Washington, Seattle, WA, USA
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Alessandro Lamorte
5Dept of Emergency Medicine, Parini Hospital, Aosta, Italy
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Marta Valente
6ISGlobal, Hospital Clínic – Universitat de Barcelona, Barcelona, Spain
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Benazir Balouch
3Dept of Pediatrics and Child Health, Aga Khan University, Karachi, Pakistan
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Carmen Muñoz Almagro
7Instituto de Recerca Pediatrica, Hospital Sant Joan de Déu, Barcelona, Spain
8Consorcio de Investigación Biomédica en Red de Epidemiología y Salud Pública (CIBERESP), Madrid, Spain
9Dept of Medicine, Universitat Internacional de Catalunya, Barcelona, Spain
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M. Imran Nisar
3Dept of Pediatrics and Child Health, Aga Khan University, Karachi, Pakistan
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Susanne May
1Dept of Biostatistics, University of Washington, Seattle, WA, USA
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Fyezah Jehan
3Dept of Pediatrics and Child Health, Aga Khan University, Karachi, Pakistan
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Quique Bassat
2Centro de Investigação em Saúde de Manhiça (CISM), Maputo, Mozambique
6ISGlobal, Hospital Clínic – Universitat de Barcelona, Barcelona, Spain
7Instituto de Recerca Pediatrica, Hospital Sant Joan de Déu, Barcelona, Spain
8Consorcio de Investigación Biomédica en Red de Epidemiología y Salud Pública (CIBERESP), Madrid, Spain
10ICREA, Barcelona, Spain
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Giovanni Volpicelli
11Dept of Emergency Medicine, San Luigi Gonzaga University Hospital, Orbassano, Italy
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  • FIGURE 1
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    FIGURE 1

    a) Flow of children with chest-indrawing pneumonia by country: Mozambique (M) and Pakistan (P). b) Flow of children with no fast breathing, no chest indrawing and no fever by country. #: 70 children in Mozambique (27.3% of screened) and 1318 children in Pakistan (81.8% of screened) met the “no chest indrawing” exclusion criterion.

  • FIGURE 2
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    FIGURE 2

    Lung ultrasound examinations consisted of longitudinal and oblique scans obtained of the anterior, lateral and posterior sides of the child's chest.

Tables

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  • TABLE 1

    Study definitions and eligibility criteria

    Definitions
     Fast breathing for ageChildren 2 to <12 months of age: RR ≥50 breaths per min
    Children ≥12 months of age: RR ≥40 breaths per min
     Severe respiratory distressGrunting, nasal flaring and/or head nodding
     WHO IMCI general danger signsLethargy or unconsciousness, convulsions, vomiting everything, inability to drink or breastfeed
    Eligibility criteria
     Inclusion criteriaChest-indrawing pneumonia cohort
     2 to 23 months of age
     Cough <14 days or difficulty breathing
     Visible indrawing of the chest wall with or without fast breathing for age
     Ability and willingness of child's caregiver to provide informed consent and to be available for follow-up for the planned duration of the study, including accepting a home visit if he/she fails to return for a scheduled study follow-up visit
    No pneumonia cohort
     2 to 23 months of age
     Cough <14 days or difficulty breathing
     Ability and willingness of child's caregiver to provide informed consent and to be available for follow-up for the planned duration of the study, including accepting a home visit if he/she fails to return for a scheduled study follow-up visit
     Exclusion criteriaChest-indrawing pneumonia cohort
     Resolution of chest indrawing after bronchodilator challenge if wheezing at screening examination
     Severe respiratory distress
     Arterial SpO2 <90% in room air, as assessed noninvasively by a pulse oximeter
     WHO IMCI general danger signs
     Stridor when calm
     Known or possible tuberculosis (history of a cough ≥14 days)
     Any medical or psychosocial condition or circumstance that, in the opinion of the investigators, would interfere with the conduct of the study or for which study participation might jeopardise the child's health
     Living outside the study catchment area
    No pneumonia cohort
     Axillary temperature ≥38°C
     Fast breathing for age
     Visible indrawing of the chest wall
     SpO2 <95% in room air, as assessed noninvasively by a pulse oximeter
     WHO IMCI general danger signs
     Stridor when calm
     Known or possible tuberculosis (history of a cough ≥14 days)
     Any medical or psychosocial condition or circumstance that, in the opinion of the investigators, would interfere with the conduct of the study or for which study participation might jeopardise the child's health
     Living outside the study catchment area

    RR: respiratory rate; WHO: World Health Organization; IMCI: Integrated Management of Childhood Illnesses; SpO2: oxyhaemoglobin saturation.

    • TABLE 2

      Baseline characteristics of enrolled and analysed children by cohort and country

      Chest-indrawing pneumonia cohortNo pneumonia cohortBetween-cohort comparison p-value
      MozambiquePakistanBetween-country comparison p-valueMozambiquePakistanBetween-country comparison p-valueMozambiquePakistan
      Subjects n981282020
      Age months10.9±6.06.8±4.8<0.0111.0±6.17.6±4.80.060.910.45
       <12 months55 (56.1%)111 (86.7%)<0.0112 (60.0%)15 (75.0%)0.500.940.18
      Female39 (39.8%)34 (26.6%)0.04914 (70.0%)12 (60.0%)0.740.03<0.01
      Temperature °C37.1±1.136.7±0.8<0.0136.3±0.636.3±0.60.72<0.010.02
       Fever (≥38°C) n (%)21 (21.4%)11 (8.6%)0.010 (0.0%)0 (0.0%)0.020.36
      Respiratory rate breaths per min
       <12 months52.5±11.453.5±7.90.5839.7±7.138.8±4.80.72<0.01<0.01
       ≥12 months44.3±10.047.6±9.60.2334.4±4.232.2±4.50.41<0.01<0.01
       Fast breathing52 (53.1%)83 (64.8%)0.100 (0.0%)0 (0.0%)<0.01<0.01
      Oxyhaemoglobin saturation %97.8±2.695.3±2.2<0.0196.2±1.596.8±1.60.23<0.01<0.01
       <90% n (%)1 (1.0%)0 (0.0%)0.430 (0.0%)0 (0.0%)>0.99
      Haemoglobin g·dL−110.0±1.310.7±1.3<0.0110.3±1.09.4±1.50.040.37<0.01
      Positive HIV rapid diagnostic test#0 (0.0%)0 (0.0%)>0.99
      Positive malaria rapid diagnostic test¶1 (1.0%)0 (0.0%)>0.99
      C-reactive protein+ µg·mL−138.8±49.8109.9±199.7<0.0118.2±33.90.03
      Procalcitonin§ ng·mL−11.7±7.20.2±0.60.07
      Streptococcus pneumoniaeƒ84 (86.6%)
      Bordetella pertussis##3 (3.1%)0 (0.0%)>0.99
      Chlamydophila pneumophila##0 (0.0%)0 (0.0%)
      Legionella pneumophila##0 (0.0%)0 (0.0%)
      Mycoplasma pneumoniae##3 (3.1%)0 (0.0%)>0.99
      Nasopharyngeal viral PCR¶¶
       Number of viruses detected1.67±1.041.08±0.65<0.011.25±0.550.01
       Any viruses detected90 (91.8%)84 (84.0%)0.1419 (95.0%)0.31
        1 virus detected41 (41.8%)61 (61.0%)13 (65.0%)
        2 viruses detected30 (30.6%)22 (22.0%)6 (30.0%)
        ≥3 viruses detected19 (19.4%)1 (1.0%)0 (0.0%)

      Data are presented as mean±sd or n (%), unless otherwise stated. #: HIV testing only conducted in Mozambique; missing for 55 children with chest-indrawing pneumonia. ¶: malaria testing only conducted in Mozambique; missing for two children with chest-indrawing pneumonia. +: C-reactive protein missing for five children with chest-indrawing pneumonia in Mozambique; in Pakistan, only measured for children with chest-indrawing pneumonia. §: procalcitonin only measured in Mozambique; missing for five children with chest-indrawing pneumonia. ƒ: S. pneumoniae carriage only tested for 97 children with chest-indrawing pneumonia in Mozambique. ##: B. pertussis, C. pneumophila, L. pneumophila and M. pneumoniae carriage only tested in Mozambique; all children with B. pertussis were also positive for S. pneumoniae, and two of the three children with M. pneumoniae were also positive for S. pneumoniae; no children were positive for both B. pertussis and M. pneumoniae. ¶¶: viral carriage in Pakistan only tested in 100 analysed children with chest-indrawing pneumonia.

      • TABLE 3

        Baseline lung ultrasound pattern by nasopharyngeal carriage in the chest-indrawing pneumonia cohort in Mozambique

        Chest-indrawing pneumonia cohort in Mozambique
        Bacteria but no viruses detectedViruses but no bacteria detectedBoth bacteria and viruses detectedCarriage type comparison p-value
        Subjects n81277
        Any consolidation4 (50.0%)1 (8.3%)10 (13.0%)0.03
         Peripheral2 (25.0%)1 (8.3%)8 (10.4%)
         Lobar2 (25.0%)1 (8.3%)2 (2.6%)
         Present in both lungs1 (12.5%)1 (8.3%)2 (2.6%)
        Any pleural effusion0 (0.0%)0 (0.0%)0 (0.0%)
        Any interstitial pattern4 (50.0%)4 (33.3%)16 (20.8%)0.14
         Focal4 (50.0%)4 (33.3%)16 (20.8%)
         Multifocal1 (12.5%)0 (0.0%)0 (0.0%)
         Present in both lungs1 (12.5%)2 (16.7%)5 (6.5%)
        Any obstructive atelectasis0 (0.0%)0 (0.0%)0 (0.0%)

        Data are presented as n (%) unless otherwise stated. Both bacterial and viral carriage assessed in Mozambique. Pakistan did not have bacterial carriage testing conducted.

        • TABLE 4

          Baseline lung ultrasound imaging patterns of children by cohort and country

          Chest-indrawing pneumonia cohortNo pneumonia cohortBetween-cohort comparison p-value
          MozambiquePakistanBetween-country comparison p-valueMozambiquePakistanBetween-country comparison p-valueMozambiquePakistan
          Subjects n981282020
          Any consolidation15 (15.3%)57 (44.5%)<0.010 (0.0%)1 (5.0%)>0.990.07<0.01
           Peripheral11 (11.2%)51 (39.8%)0 (0.0%)1 (5.0%)
           Lobar5 (5.1%)18 (14.1%)0 (0.0%)0 (0.0%)
           Present in both lungs4 (4.1%)18 (14.1%)0 (0.0%)0 (0.0%)
          Any pleural effusion0 (0.0%)2 (1.6%)0.510 (0.0%)0 (0.0%)>0.99
           Simple0 (0.0%)2 (1.6%)0 (0.0%)0 (0.0%)
           Complex0 (0.0%)0 (0.0%)0 (0.0%)0 (0.0%)
           Present in both lungs0 (0.0%)0 (0.0%)0 (0.0%)0 (0.0%)
          Any interstitial pattern24 (24.5%)80 (62.5%)<0.012 (10.0%)6 (30.0%)0.240.240.01
           Focal24 (24.5%)64 (50.0%)2 (10.0%)6 (30.0%)
           Multifocal1 (1.0%)28 (21.9%)0 (0.0%)1 (5.0%)
           Present in both lungs8 (8.2%)46 (35.9%)0 (0.0%)4 (20.0%)
          Any obstructive atelectasis0 (0.0%)3 (2.3%)0.260 (0.0%)0 (0.0%)>0.99
           Present in both lungs0 (0.0%)0 (0.0%)0 (0.0%)0 (0.0%)

          Data are presented as n (%) unless otherwise stated.

          • TABLE 5

            Inter rater reliability among lung ultrasound experts

            Chest-indrawing
            pneumonia cohort# κ
            No pneumonia cohort¶ κ
            Overall pneumonia0.9151+
            Consolidation0.9151+
            Pleural effusion1+
            Interstitial pattern0.9010.635
            Obstructive atelectasis0.746

            Testing of κ only signifies that the level of inter rater reliability differs from what would occur by chance (κ=0). Thus, p-values are not noted for κ results. #: n=226. ¶: n=40. +: based on small counts for one of the two possible categories of inter rater reliability, with two or fewer children in the smaller category.

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              Supplementary material 00518-2020.SUPPLEMENT

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            Lung ultrasound patterns in paediatric pneumonia in Mozambique and Pakistan
            Amy Sarah Ginsburg, Pio Vitorino, Zunera Qasim, Jennifer L. Lenahan, Jun Hwang, Alessandro Lamorte, Marta Valente, Benazir Balouch, Carmen Muñoz Almagro, M. Imran Nisar, Susanne May, Fyezah Jehan, Quique Bassat, Giovanni Volpicelli
            ERJ Open Research Jan 2021, 7 (1) 00518-2020; DOI: 10.1183/23120541.00518-2020

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            Lung ultrasound patterns in paediatric pneumonia in Mozambique and Pakistan
            Amy Sarah Ginsburg, Pio Vitorino, Zunera Qasim, Jennifer L. Lenahan, Jun Hwang, Alessandro Lamorte, Marta Valente, Benazir Balouch, Carmen Muñoz Almagro, M. Imran Nisar, Susanne May, Fyezah Jehan, Quique Bassat, Giovanni Volpicelli
            ERJ Open Research Jan 2021, 7 (1) 00518-2020; DOI: 10.1183/23120541.00518-2020
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