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Indoor air pollution and tobacco smoke exposure: impact on nasopharyngeal bacterial carriage in mothers and infants in an African birth cohort study

Aneesa Vanker, Polite M. Nduru, Whitney Barnett, Felix S. Dube, Peter D. Sly, Robert P. Gie, Mark P. Nicol, Heather J. Zar
ERJ Open Research 2019 5: 00052-2018; DOI: 10.1183/23120541.00052-2018
Aneesa Vanker
1Dept of Paediatrics and Child Health, Red Cross War Memorial Children's Hospital, and SAMRC Unit on Child and Adolescent Health, University of Cape Town, Cape Town, South Africa
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  • For correspondence: aneesa.vanker@uct.ac.za
Polite M. Nduru
1Dept of Paediatrics and Child Health, Red Cross War Memorial Children's Hospital, and SAMRC Unit on Child and Adolescent Health, University of Cape Town, Cape Town, South Africa
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Whitney Barnett
1Dept of Paediatrics and Child Health, Red Cross War Memorial Children's Hospital, and SAMRC Unit on Child and Adolescent Health, University of Cape Town, Cape Town, South Africa
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Felix S. Dube
2Dept of Molecular and Cell Biology, Faculty of Science, University of Cape Town, Cape Town, South Africa
3Division of Medical Microbiology, Dept of Pathology, Faculty of Health Sciences, University of Cape Town, Cape Town, South Africa
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Peter D. Sly
4Children's Health and Environment Program, Child Health Research Centre, The University of Queensland, South Brisbane, Australia
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Robert P. Gie
5Dept of Paediatrics and Child Health, Tygerberg Children's Hospital, Stellenbosch University, Cape Town, South Africa
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Mark P. Nicol
3Division of Medical Microbiology, Dept of Pathology, Faculty of Health Sciences, University of Cape Town, Cape Town, South Africa
6National Health Laboratory Service, Cape Town, South Africa
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Heather J. Zar
1Dept of Paediatrics and Child Health, Red Cross War Memorial Children's Hospital, and SAMRC Unit on Child and Adolescent Health, University of Cape Town, Cape Town, South Africa
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  • FIGURE 1
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    FIGURE 1

    Cohort description and samples collected. IAP: indoor air pollution.

  • FIGURE 2
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    FIGURE 2

    Nasopharyngeal bacterial carriage at birth, 6 months and 1 year of life.

  • FIGURE 3
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    FIGURE 3

    Multivariate analysis of antenatal exposures and maternal nasopharyngeal bacterial carriage. PM10: particulate matter <10 µm in diameter; RR: risk ratio.

Tables

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  • TABLE 1

    Maternal and infant characteristics

    Mbekweni (black African)Newman (mixed ancestry)Totalp-value
    Maternal characteristics
     Mothers530 (54%)452 (46%)982 (100%)
     Age at enrolment years26.9 (22.3, 31.6)24.6 (21.3, 29.1)25.8 (22.0, 30.6)<0.001
     HIV-infected193 (36%)13 (3%)206 (21%)<0.001
     Unemployed400 (75%)325 (72%)724 (74%)0.205
     SES quartile
      Lowest SES157 (30%)80 (18%)237 (24%)<0.001
      Low–moderate SES150 (28%)109 (24%)259 (26%)
      Moderate–high SES126 (24%)127 (28%)253 (26%)
      Highest SES97 (18%)136 (30%)233 (24%)
     Household members4 (3, 6)5 (4, 7)4 (3, 6)<0.001
     Married/cohabiting188 (35%)194 (43%)382 (39%)0.017
    Infant characteristics and birth outcomes
     Number of infants; sets of twins534 (54%); 4452 (46%); 0986 (100%); 4
     Female280 (52%)204 (45%)484 (49%)0.022
     Gestation at delivery weeks39 (38, 40)39 (37, 40)39 (38, 40)0.032
     Birthweight g3180 (2810, 3460)2990 (2630, 3340)3080 (2720, 3415)<0.001
     Weight-for-age z-score−0.4 (−1.3, 0.2)−0.7 (−1.4, −0.1)−0.6 (−1.3, 0.0)<0.001
     Birthweight <2500 g55 (10%)83 (18%)138 (14%)<0.001
     Birth <37 weeks gestation16 (3%)19 (4%)35 (4%)0.314
     Feeding at 6 months
      Exclusive breastfeeding76 (14%)66 (15%)142 (14%)<0.001
      Mixed89 (17%)170 (38%)259 (26%)
      Not breastfeeding369 (69%)216 (48%)585 (59%)
     Duration of exclusive breastfeeding months1.1 (0.5, 3.0)1.6 (0.9, 3.0)1.4 (0.7, 3.0)0.410
     Day care attendance
      6 months of age17 (3%)28 (6%)45 (5%)0.024
      12 months of age69 (13%)90 (20%)159 (16%)0.003
     Additional child under 5 years of age in household455 (85%)396 (88%)851 (86%)0.274
     Respiratory infection in prior month
      6 months of age40 (7%)37 (8%)77 (8%)0.685
      12 months of age29 (5%)22 (5%)51 (5%)0.691
     Antibiotic use in prior 6 months
      6 months of age25 (5%)38 (8%)63 (6%)0.057
      12 months of age14 (3%)13 (3%)27 (3%)0.957

    Data are presented as median (interquartile range), unless otherwise stated. SES: socioeconomic score.

    • TABLE 2

      Home environment and exposures

      MbekweniNewmanTotalp-value
      Home environment
       Household dimensions#
       Has ≤2 dimensions185 (38%)121 (27%)306 (33%)<0.001
       Has >2 dimensions302 (62%)320 (73%)622 (67%)
       Alternate fuel used (coal, wood, paraffin, gas)
        Cooking133 (31%)37 (10%)170 (21%)<0.001
        Heating127 (29%)7 (2%)134 (16%)<0.001
       Crowding
        Household size4 (3, 6)5 (4, 7)4 (3, 6)<0.001
        Persons per sleeping room3 (2, 4)3 (2, 5)3 (2, 5)0.010
      Pollutants measured: antenatal
       PM10 g·m−3 (n=755)32.0 (12.3, 64.2)35.6 (12.8, 65.6)33.4 (12.4, 65.6)0.417
        Above threshold73 (19%)65 (18%)138 (18%)0.853
       NO2 µg·m−3 (n=747)7.3 (2.6, 14.6)7.1 (3.9, 11.3)7.1 (3.4, 12.7)0.494
        Above threshold16 (4%)3 (1%)19 (3%)0.005
       Benzene µg·m−3 (n=729)4.6 (1.5, 17.9)3.9 (1.8, 8.6)4.3 (1.8, 11.0)0.475
        Above threshold183 (47%)147 (43%)330 (45%)0.244
       Toluene µg·m−3 (n=729)16.1 (5.9, 43.0)17.4 (8.2, 46.5)16.9 (7.2, 44.6)0.282
        Above threshold36 (9%)30 (9%)66 (9%)0.803
       CO mg·m−3 (n=706)0.0 (0.0, 5.1)0.0 (0.0, 8.4)0.0 (0.0, 7.6)0.144
        Above threshold39 (10%)42 (14%)81 (11%)0.095
      Pollutants measured: postnatal
       PM10 g·m−3 (n=505)30.0 (14.7, 49.7)28.4 (10.5, 53.7)29.3 (12.6, 52.5)0.364
        Above threshold38 (16%)36 (14%)74 (15%)0.499
       NO2 µg·m−3 (n=532)6.3 (2.9, 14.6)5.3 (2.6, 11.3)5.8 (2.6, 12.67)0.119
        Above threshold6 (2%)1 (0%)7 (1%)0.041
       Benzene µg·m−3 (n=462)2.8 (0.8, 14.4)3.2 (1.5, 7.6)3.1 (1.1, 9.5)0.345
        Above threshold95 (39%)75 (35%)170 (37%)0.426
       Toluene µg·m−3 (n=462)15.1 (4.9, 50.0)15.9 (6.5, 51.7)15.5 (5.9, 50.0)0.342
        Above threshold24 (10%)23 (11%)47 (10%)0.728
       CO mg·m−3 (n=502)0.0 (0.0, 0.0)0.0 (0.0, 5.6)0.0 (0.0, 0.0)0.018
        Above threshold17 (7%)30 (12%)47 (9%)0.026
      Maternal antenatal tobacco smoking
       Number of mothers530451981
       Maternal urine cotinine (n=954)512442
        <10 ng·mL−1, non-smoker181 (35%)47 (11%)228 (24%)<0.001
        10–499 ng·mL−1, passive/exposed255 (50%)155 (35%)410 (43%)
        ≥500 ng·mL−1, active smoker76 (15%)240 (54%)316 (33%)
      Infant urine cotinine
       Urine cotinine at birth or 6–10 weeks (n=763)415348
        <10 ng·mL−1184 (44%)55 (16%)239 (31%)<0.001
        10–499 ng·mL−1212 (51%)208 (60%)420 (55%)
        ≥500 ng·mL−119 (5%)85 (24%)104 (14%)

      Data are presented as median (interquartile range), unless otherwise stated. PM10: particulate matter <10 μm in diameter; NO2: nitrogen dioxide; CO: carbon monoxide. #: dimensions comprise type of home, building material, water supply, toilet facilities, kitchen type and ventilation in kitchen areas.

      • TABLE 3

        Multivariate analysis of postnatal exposures and infant nasopharyngeal bacterial carriage

        S. aureusS. pneumoniaeH. influenzaeM. catarrhalisGram negative bacilli
        AdjAdj2AdjAdj2AdjAdj2AdjAdj2AdjAdj2
        PM10
         6 months0.98 (0.57–1.70)0.95 (0.42–2.14)0.96 (0.79–1.16)0.96 (0.69–1.34)1.09 (0.85–1.40)1.68 (1.10– 2.57)0.91 (0.70–1.18)0.88 (0.57–1.35)0.61 (0.19–1.95)0.13 (0.02–1.05)
         12 months0.56 (0.13–2.48)2.23 (0.40–12.35)1.02 (0.87–1.20)0.98 (0.72–1.35)1.15 (0.88–1.51)1.09 (0.69–1.73)1.12 (0.90–1.40)1.42 (1.03–1.97)0.92 (0.11–7.59)
        NO2
         6 months0.90 (0.16–4.93)2.15×10−6 (1.39×10−7–3.32×10−5)1.32 (0.97–1.81)1.93 (0.98–3.80)0.58 (0.18–1.92)2.38×10−6 (2.62×10−7–2.16×10−5)0.96 (0.41–2.21)5.09×10−6 (6.23e×10−7–4.16×10−5)3.05 (0.48–19.48)1.77×10−5 (4.45×10−7–7.04×10−4)
         12 months2.32×10−6 (7.08×10−7–7.60×10−6)1.93×10−7 (2.74×10−9–1.35×10−5)1.07 (0.80–1.43)0.72 (0.27–1.92)0.58 (0.21–1.62)1.93×10−7 (2.74×10−9 – 1.35×10−5)15.89 (3.35–75.46)
        Benzene
         6 months0.78 (0.52–1.17)0.78 (0.33–1.83)1.01 (0.87–1.17)0.88 (0.64–1.22)0.96 (0.77–1.19)1.68 (1.10–2.57)0.95 (0.48–1.20)1.00 (0.72–1.39)0.65 (0.30–1.42)0.38 (0.13–1.09)
         12 months0.81 (0.36–1.82)1.37 (0.20–9.59)1.01 (0.89–1.15)1.17 (0.90–1.51)0.83 (0.65–1.05)0.90 (0.55–1.46)0.89 (0.74–0.09)0.92 (0.66–1.28)2.06 (0.44–9.74)
        CO
         6 months1.17 (0.74–1.87)1.53 (0.78–2.98)1.03 (0.88–1.21)1.28 (0.99–1.66)1.03 (0.80–1.33)0.99 (0.63–1.54)1.04 (0.85–1.27)1.19 (0.88–1.60)1.15 (0.48–2.75)2.15 (0.90–5.12)
         12 months0.68 (0.22–2.12)0.56 (0.08–3.97)1.05 (0.91–1.22)1.13 (0.89–1.44)1.01 (0.76–1.34)0.91 (0.58–1.43)0.98 (0.79–1.22)1.01 (0.75–1.35)1.60 (0.38–6.72)
        Smoking
         6 months1.28 (0.87–1.88)0.90 (0.44–1.83)1.14 (1.00–1.30)1.12 (0.86–1.47)0.93 (0.75–1.15)0.92 (0.62–1.37)1.01 (0.84–1.22)1.15 (0.81–1.62)0.88 (0.46–1.70)0.93 (0.34–2.62)
         12 months0.79 (0.42–1.50)0.81 (0.18–3.58)1 (0.87–1.15)0.93 (0.74–1.18)1.21 (0.96–1.53)1.43 (0.95–2.17)1.03 (0.87–1.21)1.05 (0.77–1.41)6.77 (0.91–50.53)
        Toluene
         6 months0.55 (0.24–1.27)0.86 (0.23–3.17)0.95 (0.74–1.22)1.23 (0.82–1.83)0.88 (0.61–1.27)0.52 (0.25–1.09)0.99 (0.73–1.35)5.57×10−7 (3.22×10−7–9.64×10−7)
         12 months0.82 (0.22–3.04)1.00×10−7 (1.95×10−7–5.16×10−7)1.1 (0.90–1.34)1.00 (0.70–1.43)1.15 (0.83–1.59)1.14 (0.62–2.11)1.13 (0.85–1.51)5.84×10−7 (2.08×10−7–1.64×10−6)

        Data are presented as risk ratio (95% CI). Adj: adjusted for all the clinical-demographic variables; Adj2: adjusted for all the clinical-demographic variables, plus adjusting for other indoor air pollutants. Risk ratios in bold are statistically significant at p-values derived using Benjamini–Hochberg (p<0.05). Empty cells indicate that model convergence was not achieved. PM10: particulate matter <10 μm in diameter; NO2: nitrogen dioxide; CO: carbon monoxide.

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        Indoor air pollution and tobacco smoke exposure: impact on nasopharyngeal bacterial carriage in mothers and infants in an African birth cohort study
        Aneesa Vanker, Polite M. Nduru, Whitney Barnett, Felix S. Dube, Peter D. Sly, Robert P. Gie, Mark P. Nicol, Heather J. Zar
        ERJ Open Research Feb 2019, 5 (1) 00052-2018; DOI: 10.1183/23120541.00052-2018

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        Indoor air pollution and tobacco smoke exposure: impact on nasopharyngeal bacterial carriage in mothers and infants in an African birth cohort study
        Aneesa Vanker, Polite M. Nduru, Whitney Barnett, Felix S. Dube, Peter D. Sly, Robert P. Gie, Mark P. Nicol, Heather J. Zar
        ERJ Open Research Feb 2019, 5 (1) 00052-2018; DOI: 10.1183/23120541.00052-2018
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