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Exhaled nitric oxide, nitrite/nitrate levels, allergy, rhinitis and asthma in the EGEA study

Rachel Nadif, Marta Rava, Brigitte Decoster, Hélène Huyvaert, Nicole Le Moual, Jean Bousquet, Valérie Siroux, Raphaëlle Varraso, Isabelle Pin, Farid Zerimech, Régis Matran
European Respiratory Journal 2014 44: 351-360; DOI: 10.1183/09031936.00202413
Rachel Nadif
INSERM, U1018, CESP Centre for Research in Epidemiology and Population Health, Respiratory and Environmental Epidemiology Team, Villejuif, FranceUniv. Paris-Sud, UMRS 1018, Villejuif, France
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Marta Rava
INSERM, U1018, CESP Centre for Research in Epidemiology and Population Health, Respiratory and Environmental Epidemiology Team, Villejuif, FranceUniv. Paris-Sud, UMRS 1018, Villejuif, France
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  • For correspondence: mrava@cnio.es
Brigitte Decoster
Univ. Lille Nord de France, Lille, France
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Hélène Huyvaert
Univ. Lille Nord de France, Lille, FranceLaboratoire de Biochimie, Centre de Biologie Pathologie, CHRU de Lille, Lille, France
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Nicole Le Moual
INSERM, U1018, CESP Centre for Research in Epidemiology and Population Health, Respiratory and Environmental Epidemiology Team, Villejuif, FranceUniv. Paris-Sud, UMRS 1018, Villejuif, France
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Jean Bousquet
INSERM, U1018, CESP Centre for Research in Epidemiology and Population Health, Respiratory and Environmental Epidemiology Team, Villejuif, FranceUniv. Paris-Sud, UMRS 1018, Villejuif, FranceCHU Arnaud de Villeneuve, Montpellier, France
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Valérie Siroux
Université Grenoble Alpes, Institut Albert Bonniot, Team of Environmental Epidemiology Applied to Reproduction and Respiratory Health, Grenoble, FranceINSERM, Institut Albert Bonniot, Team of Environmental Epidemiology Applied to Reproduction and Respiratory Health, Grenoble, FranceCHU de Grenoble, Institut Albert Bonniot, Team of Environmental Epidemiology Applied to Reproduction and Respiratory Health, Grenoble, France
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Raphaëlle Varraso
INSERM, U1018, CESP Centre for Research in Epidemiology and Population Health, Respiratory and Environmental Epidemiology Team, Villejuif, FranceUniv. Paris-Sud, UMRS 1018, Villejuif, France
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Isabelle Pin
Université Grenoble Alpes, Institut Albert Bonniot, Team of Environmental Epidemiology Applied to Reproduction and Respiratory Health, Grenoble, FranceINSERM, Institut Albert Bonniot, Team of Environmental Epidemiology Applied to Reproduction and Respiratory Health, Grenoble, FranceCHU de Grenoble, Institut Albert Bonniot, Team of Environmental Epidemiology Applied to Reproduction and Respiratory Health, Grenoble, France
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Farid Zerimech
Laboratoire de Biochimie, Centre de Biologie Pathologie, CHRU de Lille, Lille, France
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Régis Matran
Univ. Lille Nord de France, Lille, France
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  • Figure 1–
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    Figure 1–

    Concordance of ever asthma, allergic sensitisation (positive skin prick test, SPT+) and current rhinitis (proportional Venn diagram). Data on current rhinitis was missing for four participants without allergic sensitisation and asthma, one participant with asthma and one participant with allergic sensitisation (n=517).

  • Figure 2–
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    Figure 2–

    Associations between exhaled nitric oxide fraction (FeNO), total NO2−/NO3− and (NO2− + NO3−)/NO ratio levels in exhaled breath condensate with allergic sensitisation, current rhinitis and both. Regression coefficients (beta) and 95% confidence intervals for associations between FeNO, total NO2−/NO3− levels, (NO2− + NO3−)/NO ratio and allergic sensitisation, current rhinitis and both, estimated through generalised estimating equation linear regression methods, and adjusted for covariates: age, sex, smoking, ambient ozone concentration, asthma and centre for NO2−/NO3− level; age, sex, smoking, height, asthma and centre for FeNO level; age, sex, smoking, asthma and centre for (NO2− + NO3−)/NO ratio. SPT+: positive skin prick test, i.e. a mean wheal diameter ≥3 mm than the negative control for at least one of 12 aeroallergens.

Tables

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  • Table 1– Characteristics of subjects according to asthma status
    All subjectsSubjects without asthmaSubjects with asthmap-value
    Subjects n523268255
    Age years39.9±16.643.2±15.936.5±16.8<0.0001
    Sex female %51.057.544.30.003
    Body mass index kg·m−223.7±3.923.8±3.823.5±4.00.4
    Smoking habits %
     Never smokers51.649.653.7
     Ex-smokers25.328.022.40.3
     Current smokers23.122.423.9
    Asthma %
     Ever asthma48.7100.0
     Current asthma40.583.1
    Age at asthma onset %237
     0–4 years36.7
     4–16 years39.7
     >16 years23.6
    Symptomatic score#1.17±1.35 (517)0.51±0.81 (266)1.86±1.46 (251)<0.0001
    Asthma control (GINA 2006) %
     Controlled20.642.3
     Partly controlled10.722.0
     Uncontrolled8.216.9
    Eosinophilia (cells >5%) %12.46.718.4<0.0001
    Eosinophilic asthma (≥250 cells per mm2) %36.5
    FEV1 % pred103.4±17.2108.5±16.698.0±17.5<0.0001
    Methacholine test¶ (PD20 ≤4 mg) %45.428.865.1<0.0001
    Inhaled corticosteroids past 12 months %20.62.240.0<0.0001
    Inhaled corticosteroids past 3 months %7.30.014.9
    SPT+ and current rhinitis
     SPT+ %58.138.878.4<0.0001
     SPTQ (median number of SPT+)1 (0–3)0 (0–1)2 (1–4)<0.0001
     Current rhinitis %39.222.356.9<0.0001
     SPT+ and current rhinitis %32.918.048.6<0.0001
    Biological phenotypes (geometric means)
     EBC NO2−/NO3− μmol per mg proteins2.25 (1.12–4.98)2.33 (1.15–4.81)2.16 (1.13–5.11)0.5
     FeNO ppb15.1 (10.0–23.0)13.2 (9.00–18.8)17.5 (11.5–29.6)<0.0001
     EBC (NO2− + NO3−)/NO ratio (median)0.30 (0.04–0.60)0.34 (0.06–0.61)0.26 (0.04–0.58)0.16
     Plasma NO2−/NO3− μM39.1 (28.0–53.7) (510)38.9 (26.3–56.4) (263)39.3 (29.1–53.2) (247)0.8
     Eosinophil cells per mm3170 (100–280) (505)145 (100–200) (256)199 (100–300) (249)<0.0001
     IgE IU·mL−181.7 (28.8–226)49.8 (19.4–128)137 (59.0–332)<0.0001
    • Data are presented as mean±sd, unless otherwise stated. Medians and geometric means are shown with interquartile ranges. Values of n are present in italics when differing from total n. GINA: Global Initiative for Asthma; FEV1: forced expiratory volume in 1 s; PD20: provocative dose causing a 20% fall in FEV1; SPT+: positive skin prick test, i.e. a mean wheal diameter ≥3 mm than the negative control for at least one of 12 aeroallergens; SPTQ: quantitative SPT score; EBC: exhaled breath condensate; FeNO: exhaled nitric oxide fraction; Ig: immunoglobulin. #: symptomatic score is based on the number of asthma symptoms (wheeze and breathlessness, woken with chest tightness, woken by attack of shortness of breath, attack of shortness of breath at rest, attack of shortness of breath after exercise); ¶: methacholine challenge test was not performed if baseline FEV1 <80% pred.

  • Table 2– Pairwise association of exhaled breath condensate (EBC) NO2−/NO3−, exhaled nitric oxide fraction (FeNO) levels and eosinophil count in all subjects, and according to allergic sensitisation
    EBC NO2−/NO3− level μmol per mg proteins#FeNO level ppb¶
    nEstimatesdp-valuenEstimatesdp-value
    All subjects
     Eosinophil cells per mm34920.140.090.105050.250.04<0.0001
     FeNO level ppb5100.140.080.10
    Non-sensitised subjects
     Eosinophil cells per mm32040.150.130.32080.150.050.01
     FeNO level ppb215−0.170.150.3
    Sensitised subjects
     Eosinophil cells per mm32880.150.110.22970.310.06<0.0001
     FeNO level ppb2950.210.100.04
    • #: adjusted for age, sex, smoking, ambient ozone concentration, asthma and centre; ¶: adjusted for age, sex, smoking, height, asthma and centre (generalised estimating equation linear regression methods).

  • Table 3– Associations between exhaled nitric oxide fraction (FeNO), total NO2−/NO3− and ratio levels in exhaled breath condensate (EBC) with eosinophilic asthma and age at onset
    EBC NO2−/NO3− level μmol per mg proteins#FeNO level ppb¶(NO2−+NO3−)/NO ratio level+
    nGM95% CIp-valuenGM95% CIp-valuenMean95% CIp-value
    Eosinophilic asthma
     No1621.971.61–2.4116215.413.7–17.21620.250.16–0.34
     Yes932.541.98–3.260.129322.019.0–25.50.0002930.300.22–0.390.4
    Age at onset
     0–4 years872.491.93–3.218717.715.1–20.6870.330.22–0.43
     4–16 years942.091.60–2.750.3§9417.815.3–20.70.7§940.250.14–0.350.4§
     >16 years561.991.38–2.875616.813.6–20.8560.260.11–0.41
    Model adjusted for all covariates
    Eosinophilic asthma
     No1571.791.35–2.3716216.814.6–19.41620.200.09–0.32
     Yes922.301.66–3.180.139323.920.2–28.3<0.0001930.270.14–0.400.3
    Age at onset
     0–4 years842.261.60–3.208718.815.6–22.6870.300.17–0.43
     4–16 years931.911.37–2.670.15§9419.416.3–23.10.9§940.210.08–0.340.15§
     >16 years561.591.02–2.005618.414.6–23.3560.170.01–0.34
    • GM: geometric mean. #: adjusted for age, sex, smoking, ambient ozone concentration, asthma and centre; ¶: adjusted for age, sex, smoking, height, asthma and centre (generalised estimating equation regression methods); +: adjusted for age, sex, smoking, asthma and centre; §: p-value for trend.

  • Table 4– Associations between exhaled nitric oxide fraction (FeNO), total NO2−/NO3− and ratio levels in exhaled breath condensate (EBC) with allergic sensitisation
    EBC NO2−/NO3− level μmol per mg proteins#FeNO level ppb¶(NO2− + NO3−)/NO ratio level+
    nGM95% CIp-valuenGM95% CIp-valuenMean95% CIp-value
    Allergic sensitisation
     No2192.031.73–2.3821912.611.6–13.62190.2911.6–13.6
     Yes3042.412.11–2.760.1030417.315.9–18.8<0.00013040.3115.9–18.80.7
    Current rhinitis
     No3122.201.93–2.5131213.812.8–14.83120.300.25–0.36
     Yes2052.301.94–2.720.720517.716.1–19.6<0.00012050.290.22–0.360.8
    SPT+ and current rhinitis
     No2192.031.73–2.3821912.611.6–13.62190.290.22–0.36
     SPT+1312.341.90–2.890.10§13115.914.0–18.0<0.0001§1310.290.21–0.380.6§
     Both1722.472.07–2.9417218.416.5–20.51720.320.25–0.39
    Model adjusted for centre only
     Allergic sensitisation
      No2191.871.55–2.2621914.212.8–15.72190.250.17–0.33
      Yes3042.261.92–2.660.0630419.417.7–21.1<0.00013040.270.20–0.340.6
     Current rhinitis
      No3121.971.66–2.3331215.213.9–16.73120.250.18–0.32
      Yes2052.261.87–2.720.1920520.118.2–22.2<0.00012050.270.19–0.350.7
     SPT+ and current rhinitis
      No2191.871.55–2.2621914.212.8–15.72190.250.17–0.33
      SPT+1312.121.70–2.640.04§13117.515.6–19.8<0.0001§1310.240.15–0.340.4§
      Both1722.371.94–2.8917220.718.6–23.01720.290.20–0.37
    Model adjusted for all covariates
     Allergic sensitisation
      No2151.721.38–2.1421914.813.3–16.52190.210.13–0.30
      Yes2952.361.96–2.840.00830418.316.7–20.00.00063040.290.22–0.360.10
     Current rhinitis
      No3051.901.57–2.3131215.414.0–16.93120.240.16–0.31
      Yes1992.311.87–2.840.0920519.217.4–21.20.00012050.280.20–0.360.3
     SPT+ and current rhinitis
      No2151.711.37–2.1321914.813.3–16.52190.210.12–0.29
      SPT+1282.171.70–2.760.005§13116.414.6–18.4<0.0001§1310.260.17–0.360.06§
      Both1662.502.01–3.1217219.717.7–21.91720.320.23–0.40
     Allergic sensitisation (indoor only)
      No2151.661.28–2.1621914.212.7–15.92190.210.10–0.31
      Yes762.031.47–2.810.28017.114.8–19.70.02800.260.13–0.400.4
     Allergic sensitisation (outdoor only)
      No2151.661.28–2.1521914.613.2–16.32190.200.09–0.31
      Yes451.781.21–2.620.74617.214.6–20.20.06460.200.03–0.360.9
     Allergic sensitisation (moulds only)
      No2171.581.20–2.0621914.513.0–16.22190.180.07–0.30
      Yes73.961.69–9.290.04721.214.6–30.60.0670.490.11–0.870.12
    • GM: geometric mean; SPT+: positive skin prick test, i.e. a mean wheal diameter ≥3 mm than the negative control for at least one of 12 aeroallergens. #: adjusted for age, sex, smoking, ambient ozone concentration, asthma and centre; ¶: adjusted for age, sex, smoking, height, asthma and centre (generalised estimating equation regression methods); +: adjusted for age, sex, smoking, asthma and centre; §: p-value for trend.

Additional Files

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    Files in this Data Supplement:

    • J. Bousquet
    • I. Pin
    • M. Rava
    • V. Siroux
  • Supplementary material

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

    Files in this Data Supplement:

    • Supplementary material - Supplementary data, Table S1, Figure S1
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Exhaled nitric oxide, nitrite/nitrate levels, allergy, rhinitis and asthma in the EGEA study
Rachel Nadif, Marta Rava, Brigitte Decoster, Hélène Huyvaert, Nicole Le Moual, Jean Bousquet, Valérie Siroux, Raphaëlle Varraso, Isabelle Pin, Farid Zerimech, Régis Matran
European Respiratory Journal Aug 2014, 44 (2) 351-360; DOI: 10.1183/09031936.00202413

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Exhaled nitric oxide, nitrite/nitrate levels, allergy, rhinitis and asthma in the EGEA study
Rachel Nadif, Marta Rava, Brigitte Decoster, Hélène Huyvaert, Nicole Le Moual, Jean Bousquet, Valérie Siroux, Raphaëlle Varraso, Isabelle Pin, Farid Zerimech, Régis Matran
European Respiratory Journal Aug 2014, 44 (2) 351-360; DOI: 10.1183/09031936.00202413
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