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Unilateral diaphragmatic paralysis: inspiratory muscles, breathlessness and exercise capacity

Mayra Caleffi Pereira, Letícia Z. Cardenas, Jeferson G. Ferreira, Vinícius C. Iamonti, Pauliane Vieira Santana, André Apanavicius, Pedro Caruso, Angelo Fernandez, Carlos R.R. de Carvalho, Daniel Langer, André L.P. de Albuquerque
ERJ Open Research 2021 7: 00357-2019; DOI: 10.1183/23120541.00357-2019
Mayra Caleffi Pereira
1Pulmonary Division, Heart Institute (InCor), Hospital das Clínicas HCFMUSP, Faculdade de Medicina, Universidade de São Paulo, São Paulo, Brazil
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  • ORCID record for Mayra Caleffi Pereira
Letícia Z. Cardenas
1Pulmonary Division, Heart Institute (InCor), Hospital das Clínicas HCFMUSP, Faculdade de Medicina, Universidade de São Paulo, São Paulo, Brazil
2Intensive Care Unit, AC Camargo Cancer Center, São Paulo, Brazil
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Jeferson G. Ferreira
1Pulmonary Division, Heart Institute (InCor), Hospital das Clínicas HCFMUSP, Faculdade de Medicina, Universidade de São Paulo, São Paulo, Brazil
2Intensive Care Unit, AC Camargo Cancer Center, São Paulo, Brazil
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Vinícius C. Iamonti
1Pulmonary Division, Heart Institute (InCor), Hospital das Clínicas HCFMUSP, Faculdade de Medicina, Universidade de São Paulo, São Paulo, Brazil
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Pauliane Vieira Santana
1Pulmonary Division, Heart Institute (InCor), Hospital das Clínicas HCFMUSP, Faculdade de Medicina, Universidade de São Paulo, São Paulo, Brazil
2Intensive Care Unit, AC Camargo Cancer Center, São Paulo, Brazil
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André Apanavicius
1Pulmonary Division, Heart Institute (InCor), Hospital das Clínicas HCFMUSP, Faculdade de Medicina, Universidade de São Paulo, São Paulo, Brazil
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Pedro Caruso
1Pulmonary Division, Heart Institute (InCor), Hospital das Clínicas HCFMUSP, Faculdade de Medicina, Universidade de São Paulo, São Paulo, Brazil
2Intensive Care Unit, AC Camargo Cancer Center, São Paulo, Brazil
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Angelo Fernandez
3Thoracic Surgery Division, InCor, Hospital das Clínicas HCFMUSP, Faculdade de Medicina, Universidade de São Paulo, São Paulo, Brazil
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Carlos R.R. de Carvalho
1Pulmonary Division, Heart Institute (InCor), Hospital das Clínicas HCFMUSP, Faculdade de Medicina, Universidade de São Paulo, São Paulo, Brazil
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Daniel Langer
4Faculty of Kinesiology and Rehabilitation Sciences, Dept of Rehabilitation Sciences, Research Group for Cardiovascular and Respiratory Rehabilitation, KU Leuven – University of Leuven, and Respiratory Rehabilitation and Respiratory Division, University Hospital Leuven, Leuven, Belgium
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André L.P. de Albuquerque
1Pulmonary Division, Heart Institute (InCor), Hospital das Clínicas HCFMUSP, Faculdade de Medicina, Universidade de São Paulo, São Paulo, Brazil
5Sírio-Libanês Teaching and Research Institute, São Paulo, Brazil
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  • For correspondence: alpalbuquerque@hotmail.com
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  • FIGURE 1
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    FIGURE 1

    Illustration of oesophageal (Poes), gastric (Pga), transdiaphragmatic (Pdi) pressure curves during sniff manoeuvre in a patient with unilateral diaphragm paralysis (a,b) and in a healthy control subject (c,d).

  • FIGURE 2
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    FIGURE 2

    Metabolic and respiratory variables during incremental cycling exercise in patients with unilateral diaphragmatic paralysis (paralysis group) and healthy control group (CG). a) Peak oxygen uptake (V′O2), b) Ventilation (VE), c) Tidal volume (VT), d) respiratory rate (RR), e) Borg score for dyspnoea and f) Borg score for leg effort. Dotted lines represent the peak of exercise for each group. Values represent mean±sem. *p<0.05 for paralysis group versus CG at iso-work rate or peak of exercise.

  • FIGURE 3
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    FIGURE 3

    Inspiratory oesophageal (Poes), gastric (Pga), transdiaphragmatic (Pdi) pressures (a–c) and percentage of maximal scalene (EMGsca/ EMGsca, max) and sternocleidomastoid (EMGscm/ EMGscm, max) muscle activation (d, e) during incremental cycling exercise in patients with unilateral diaphragmatic paralysis (paralysis group) and healthy control group (CG). Dotted lines represent the peak of exercise for each group. Values represent mean±sem. *p<0.05 for paralysis group versus control group at iso-work rate or peak of exercise.

  • FIGURE 4
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    FIGURE 4

    Percentage of maximal oesophageal pressure generation (Poes/Poes,max) (a); percentage of maximal scalene activation (EMGsca/ EMGsca, max) (b); transdiaphragmatic pressure (Pdi) (c); and Borg score for dyspnoea (d) during incremental cycling exercise in patients with unilateral diaphragmatic paralysis (paralysis group) and healthy control group (CG) at similar ventilation. VE: ventilation. Dotted lines represent the peak of exercise for each group. Values represent mean±sem. *: p<0.05 for paralysis group versus control group at similar VE or peak of exercise (matching symbols).

Tables

  • Figures
  • TABLE 1

    Demographic data of patients with unilateral diaphragmatic paralysis and control group

    Paralysis groupControl groupp-value
    Male17 (49)10 (50)0.92
    Age years55.8±9.9 (32–77)49.8±6.4 (40–58)0.03
    Weight kg75.5±11.8 (48–99)78.7±9.8 (65–105)0.32
    Height m1.63±0.1 (1.5–1.9)1.68 ±0.1 (1.5–1.9)0.07
    BMI kg·m−228.4±3.4 (22.2–35.6)27.9±2.1(22.5–29.8)0.49
    Left paralysis22 (63)––
    Cause of paralysis
     Idiopathic10 (29)––
     Trauma13 (37)––
     After cardiac surgery8 (23)––
     After thoracic surgery4 (11)––

    Data are presented as mean±sd (range) or n (%), unless otherwise stated. BMI: body mass index.

    • TABLE 2

      Lung function and dyspnoea assessment of patients with unilateral diaphragmatic paralysis and control group at rest

      Paralysis groupControl groupp-value
      Lung function
       FEV1 sitting L (% pred)1.8±0.6 (59±13)2.9±0.5 (92±9)<0.001
       FVC sitting L (% pred)2.3±0.8 (62±13)3.5±0.7 (92±8)<0.001
       FEV1/ FVC %80±1182±50.24
       FVC supine L (% pred)2.0±0.7 (56±13)––
       Δ FVC sitting versus supine %−12±8––
       IC L (% pred)1.7±0.5 (64±13)2.7±0.5 (87±14)<0.001
       MVV L (% pred)82.1±22.8 (65±13)120.0±30.9 (85± 20)<0.001
       TLC L (% pred)4.2±0.9 (73±21)––
       DLCO (% pred)20.1±8.3 (66±38)––
       DL/VA (% pred)5.28±1.50 (107±35)––
      MRC
       111 (31)20 (100)<0.001
       214 (40)0 (0)–
       39 (26)0 (0)–
       41 (3)0 (0)–
       50 (0)0 (0)–

      Data are presented as mean±sd or n (%), unless otherwise stated. FEV1: forced expiratory volume in 1 s; % pred: % predicted; FVC: forced vital capacity, IC: inspiratory capacity; MVV: maximal voluntary ventilation; TLC: total lung capacity, DLCO: carbon monoxide diffusing capacity; DL/VA: carbon monoxide diffusing capacity by alveolar ventilation coefficient; MRC: Medical Research Council Breathlessness Scale.

      • TABLE 3

        Respiratory muscle strength of patients with unilateral diaphragmatic paralysis and control group

        Paralysis groupControl groupp-value
        Volitional inspiratory muscle strength
         PImax cmH2O (% pred)−67±25 (55±23)−103±30 (100±21)<0.001
         SNIP cmH2O (% pred)57±18 (58±15)96±20 (89±28)<0.001
         Sniff Poes cmH2O−44±13−66±260.001
         Sniff Pga cmH2O−10±936±14<0.001
         Sniff Pdi cmH2O34±17102±26<0.001
        Nonvolitional inspiratory muscle strength
         Twitch Pdi (bilateral) cmH2O5.3±2.715.3±5.7<0.001
         Twitch Pdi cmH2OUnaffected hemidiaphragm/right for control group3.5±1.37.4±2.7<0.001
         Twitch Pdi cmH2OAffected hemidiaphragm/left for control group2.5±1.18.9±3.4<0.001

        Data are presented as mean±sd, unless otherwise stated. PImax: maximal static inspiratory pressure; SNIP: sniff nasal inspiratory pressure; Sniff Poes: oesophageal pressure during sniff manoeuvre; Sniff Pga: gastric pressure during sniff manoeuvre; Sniff Pdi: transdiaphragmatic pressure during sniff manoeuvre; Twitch Pdi: transdiaphragmatic pressure during phrenic nerve magnetic stimulation.

        • TABLE 4

          Metabolic, respiratory, and cardiovascular parameters recorded at peak of incremental cardiopulmonary exercise testing (CPET) in patients with unilateral diaphragmatic paralysis and control group

          Paralysis groupControl groupp-value
          CPET performance
           Work rate W (% pred)83.9±38.5 (54±26)152.3±55.2 (90±41)<0.001
           V′O2 mL·kg−1·min−1 (% pred)18.7±5.5 (90.2±20.1)25.3±9.5 (106.7±21.8)0.01
           RER0.99±0.131.09±0.090.01
          Ventilation and gas exchange
           VT L1.3±0.51.9±0.4<0.001
           VT/IC %72±1172±80.93
           VE L·min−151.5±16.974.7±23.70.001
           RR bpm42±939±90.24
           VE/MVV0.6±0.30.6±0.20.44
           IC L1.6±0.42.8±0.5<0.001
           Δ IC (peak-rest) L0.0±0.20.6±10.03
           VE/VCO236±535±30.86
           SpO2 %93±395±10.06
          Cardiovascular
           HR bpm (% pred)138±22 (85±12)157±19 (93±10)0.003
           O2 pulse mL·bpm−1 (% pred)14±3 (82±21)15±5 (89±28)0.15
          Symptoms
           Borg modified (dyspnoea)9 (7–10)5 (3.25–9)0.001
           Borg modified (legs effort)9 (7–10)7 (5–8.75)0.02

          Data are presented as mean±sd and median (25th–75th percentile), unless otherwise stated. V′O2: maximal oxygen consumption; RER: respiratory exchange ratio; VT: tidal volume; VE: pulmonary ventilation; RR: respiratory rate; MVV: maximum voluntary ventilation; IC: inspiratory capacity; VCO2: CO2 production; SpO2: peripheral oxygen saturation; HR: heart rate.

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          Unilateral diaphragmatic paralysis: inspiratory muscles, breathlessness and exercise capacity
          Mayra Caleffi Pereira, Letícia Z. Cardenas, Jeferson G. Ferreira, Vinícius C. Iamonti, Pauliane Vieira Santana, André Apanavicius, Pedro Caruso, Angelo Fernandez, Carlos R.R. de Carvalho, Daniel Langer, André L.P. de Albuquerque
          ERJ Open Research Jan 2021, 7 (1) 00357-2019; DOI: 10.1183/23120541.00357-2019

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          Unilateral diaphragmatic paralysis: inspiratory muscles, breathlessness and exercise capacity
          Mayra Caleffi Pereira, Letícia Z. Cardenas, Jeferson G. Ferreira, Vinícius C. Iamonti, Pauliane Vieira Santana, André Apanavicius, Pedro Caruso, Angelo Fernandez, Carlos R.R. de Carvalho, Daniel Langer, André L.P. de Albuquerque
          ERJ Open Research Jan 2021, 7 (1) 00357-2019; DOI: 10.1183/23120541.00357-2019
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