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

ERJ Open Research, Volume 5, No. 1, Year 2019

Interpretation

Indoor air pollution (IAP) or environmental tobacco smoke (ETS) exposure may influence nasopharyngeal carriage of bacterial species and development of lower respiratory tract infection (LRTI). The aim of this study was to longitudinally investigate the impact of antenatal or postnatal IAP/ETS exposure on nasopharyngeal bacteria in mothers and infants. A South African cohort study followed mother–infant pairs from birth through the first year. Nasopharyngeal swabs were taken at birth, 6 and 12 months for bacterial culture. Multivariable and multivariate Poisson regression investigated associations between nasopharyngeal bacterial species and IAP/ETS. IAP exposures (particulate matter, carbon monoxide, nitrogen dioxide, volatile organic compounds) were measured at home visits. ETS exposure was measured through maternal and infant urine cotinine. Infants received the 13-valent pneumococcal and Haemophilus influenzae B conjugate vaccines. There were 881 maternal and 2605 infant nasopharyngeal swabs. Antenatal ETS exposure was associated with Streptococcus pneumoniae carriage in mothers (adjusted risk ratio (aRR) 1.73 (95% CI 1.03–2.92)) while postnatal ETS exposure was associated with carriage in infants (aRR 1.14 (95% CI 1.00–1.30)) Postnatal particulate matter exposure was associated with the nasopharyngeal carriage of H. influenzae (aRR 1.68 (95% CI 1.10– 2.57)) or Moraxella catarrhalis (aRR 1.42 (95% CI 1.03–1.97)) in infants. Early-life environmental exposures are associated with an increased prevalence of specific nasopharyngeal bacteria during infancy, which may predispose to LRTI. This study was nested within the Drakenstein Child Health Study (DCHS), a birth cohort in a peri-urban area of South Africa [12]. Consenting pregnant women were enrolled at 20–28 weeks’ gestation at two public primary health clinics: Mbekweni (serving a predominantly black African population) and Newman (serving a predominantly mixed ancestry population) from March 2012 to July 2015. All births occurred at a single, central hospital, Paarl hospital. Thereafter, mother–infant pairs were followed at 6, 10 and 14 weeks, 6, 9 and 12 months, for healthcare and immunisations including the 13-valent pneumococcal conjugate vaccine (PCV-13) given at 6, 14 weeks and 9 months and Haemophilus influenzae type b conjugate vaccine at 6, 10, 14 weeks according to the South African Expanded Programme on Immunisation schedule [13]. Study questionnaires and clinical data were collected at enrolment and follow-up visits. A validated socioeconomic score (SES) was used to categorise participants into quartiles as lowest, low-moderate, moderate-high or highest SES [5]. Clinical data collected at each follow-up visit included details on recent respiratory tract infections, including respiratory symptoms, otitis media, wheeze or LRTIs in the preceding month and any antibiotic use in the prior 6 months. The participant’s home environment was assessed and dwellings categorised based on having two or more defined household dimensions (type of home, building material, water supply, toilet facilities, kitchen type, ventilation in kitchen areas) [5]. IAP was measured at home visits conducted antenatally (within 4 weeks of enrolment) and postnatally (between 4–6 months of the infant’s life) [5]. Home visits were conducted over 3 years with sampling occurring throughout the year covering all seasons and weather conditions. PM10 and CO were measured by separate monitors (AirChek 52; SKC, Eighty-Four, PA, USA for PM10 and Altair; Troy, MI, USA for CO) left in homes over 24 h. NO2 and VOCs, benzene and toluene, were measured using diffusion tubes (Radiello absorbent filters in polyethylene diffusive body; Sigma-Aldrich, St Louis, MO, USA) and (Markes thermal desorption tubes; Llantrisant, UK) left in homes for 2 weeks [5]. These monitors were internally calibrated for temperature and humidity as per the manufacturer information, whereas diffusion tubes were corrected for humidity during laboratory analysis [5, 14]. The South African National Ambient Air Quality Standards were used to define expected exposure levels for each pollutant based on an averaging period of 1 year for each measure [15, 16]. Maternal, paternal and household tobacco smoking and exposure were assessed using questionnaires administered at enrolment, and antenatal and postnatal visits. These were validated using maternal and infant urine cotinine measures. Maternal cotinine was measured antenatally and at birth, and infant cotinine at birth and 6–10 week with the highest result used to assign smoking status and exposure. Cotinine levels were classified as <10 ng·mL−1 (nonsmoker), 10–499 ng·mL−1 (passive smoker/exposed), or ≥500 ng·mL−1 (active smoker) [7]. Nasopharyngeal swabs were obtained from mothers (at the time of delivery) and infants at birth, 6 and 12 months by trained study staff according to World Health Organization recommendations [17]. The swabs were immediately stored in 1 mL of skimmed milk, tryptone, glucose and glycerol transport medium (STGG), transported on ice to the laboratory and frozen at −80°C for later batch processing. After thawing at room temperature (22°C), samples were vortexed for 15 s before plating out a 10 µL aliquot onto four different solid media (National Health Laboratory Services, Green Point Media Laboratory Cape Town, South Africa). Standard laboratory protocols were used for the phenotypic and biochemical identification of common bacterial species that asymptomatically colonise the upper respiratory tract. For S. pneumoniae culture, Columbia blood agar base with 2% agar, 5% horse blood and 4 mg·mL−1 gentamicin (CAG) was incubated at 37°C in 5% CO2 overnight. Presumptive S. pneumoniae isolates were identified by colony morphology, α-haemolysis, optochin disk susceptibility (Oxoid, Basingstoke, UK) and confirmed using lytA PCR [18]. For H. influenzae, bacitracin heated blood agar plates were incubated at 37°C with 5% carbon dioxide (CO2). Suspected H. influenzae colonies were inoculated onto Columbia agar and identified using Factors X, V and XV discs and by observing growth in the haemolytic zone of Staphylococcus aureus on blood agar plates. S. aureus isolates were identified by culturing on mannitol salt agar, and DNase testing whereas Moraxella catarrhalis isolates were identified by culturing on 2% blood agar and incubated overnight at 37°C. Isolates were presumptively identified by push test and confirmed by copB PCR [19]. Gram-negative bacteria were subcultured onto MacConkey agar and identified on Vitek 2® (bioMérieux, Marcy I'Etoile, France). The study was approved by the Human Research Ethics Committees of the Faculties of Health Sciences, University of Cape Town and Stellenbosch University, and by the Western Cape Provincial Health Research committee (HREC 149/2013). Mothers provided written informed consent at enrolment. Study data were captured in a relational Microsoft Access® database or collected and managed using REDCap electronic data capture tools hosted at the University of Cape Town [20]. Statistical analyses were conducted in Stata version 14.2 for Windows (Stata Corp, College Station, TX, USA). Statistical tests were considered significant if the p-value was <0.05 or if p-value cut-offs were derived using the Benjamini–Hochberg procedure for assessing the association between IAP and the pathogens [21]. Categorical variables were summarised using frequency counts and percentages, n (%). Normally and non-normally distributed continuous variables were described using mean (sd) and median (interquartile range (IQR)) values, respectively. Mann–Whitney or Wilcoxon signed-rank tests, as appropriate, were used to compare medians as well as their spread. Cross tabulations with Fishers’ exact or Chi-squared tests were used to describe and compare the prevalence of pathogen carriage between the infants (at all time points) and their mothers or between different time points for infants. Multivariable modified Poisson regression analyses with robust error variance [22] were performed to estimate adjusted risk ratios (aRRs) between each bacterial pathogen and IAP measures (individually (adjusted) or together (adjusted 2)). The association between antenatal exposures or maternal cotinine and maternal carriage was explored as was the association between postnatal exposure or infant cotinine and infant carriage. The multivariable Poisson regressions adjusted for demographic and clinical factors (weight-for-age z-score at birth, preterm, ethnicity, sex, HIV exposure, time on exclusive breastfeeding, average number of people per sleeping room, dwelling category, recent respiratory infection, day care attendance, vaccination, number of other children under 5 years in the household, antibiotic use) that have been associated with pathogen acquisition. Multivariable regressions were then further performed for each site [23, 24]. Further, we explored the possible confounding effects of bacterial co-carriage by including indicator variables for each pathogen.

AI Digest

Study Justification:

This study aimed to investigate the impact of indoor air pollution (IAP) and environmental tobacco smoke (ETS) exposure on nasopharyngeal bacterial carriage in mothers and infants. The study is important because IAP and ETS exposure have been linked to the development of lower respiratory tract infections (LRTI). Understanding the relationship between these exposures and nasopharyngeal bacteria can provide valuable insights into the prevention and management of LRTIs in infants.

Highlights:

– The study followed mother-infant pairs from birth through the first year, collecting nasopharyngeal swabs at birth, 6 months, and 12 months for bacterial culture.
– Antenatal ETS exposure was associated with Streptococcus pneumoniae carriage in mothers, while postnatal ETS exposure was associated with carriage in infants.
– Postnatal particulate matter exposure was associated with the nasopharyngeal carriage of Haemophilus influenzae or Moraxella catarrhalis in infants.
– The study found that early-life environmental exposures are associated with an increased prevalence of specific nasopharyngeal bacteria during infancy, which may predispose to LRTI.

Recommendations:

Based on the findings of this study, the following recommendations can be made:

1. Public health interventions should focus on reducing exposure to indoor air pollution and environmental tobacco smoke, especially during pregnancy and infancy.
2. Health education programs should raise awareness about the potential risks of indoor air pollution and tobacco smoke exposure on respiratory health, particularly for pregnant women and parents of infants.
3. Further research is needed to explore the long-term effects of nasopharyngeal bacterial carriage on the development of lower respiratory tract infections and to identify effective preventive strategies.

Key Role Players:

To address the recommendations, the following key role players are needed:

1. Public health authorities and policymakers: They play a crucial role in implementing policies and regulations to reduce indoor air pollution and tobacco smoke exposure.
2. Healthcare professionals: They can provide education and counseling to pregnant women and parents about the risks of exposure and promote healthy behaviors.
3. Researchers: Further studies are needed to deepen our understanding of the relationship between indoor air pollution, tobacco smoke exposure, and respiratory health.

Cost Items:

While the actual cost of implementing the recommendations cannot be estimated without detailed planning, the following cost items should be considered:

1. Research funding: Funding is needed to support further research on the topic, including data collection, analysis, and publication.
2. Public health campaigns: Budgets should be allocated for the development and implementation of health education programs targeting pregnant women and parents.
3. Monitoring and enforcement: Resources are required to monitor compliance with regulations on indoor air pollution and tobacco smoke exposure and enforce penalties if necessary.
Please note that the above cost items are general categories and the specific costs will vary depending on the context and scope of the interventions.

Strength of Evidence

The strength of evidence for this abstract is 7 out of 10.
The evidence in the abstract is moderately strong, but there are some areas for improvement. The study design is a cohort study, which provides a higher level of evidence compared to other study designs. The study collected data from a large number of participants and used multivariable and multivariate Poisson regression to investigate associations between nasopharyngeal bacterial species and indoor air pollution (IAP) or environmental tobacco smoke (ETS) exposure. The study also measured various pollutants and cotinine levels to assess exposure levels accurately. However, the abstract does not provide information on the representativeness of the study population or the generalizability of the findings. Additionally, the abstract does not mention any limitations of the study or potential sources of bias. To improve the strength of the evidence, it would be helpful to include information on the representativeness of the study population and any limitations or potential sources of bias. This would provide a clearer understanding of the study’s findings and their applicability to other populations.

Abstract

This study was nested within the Drakenstein Child Health Study (DCHS), a birth cohort in a peri-urban area of South Africa [12]. Consenting pregnant women were enrolled at 20–28 weeks’ gestation at two public primary health clinics: Mbekweni (serving a predominantly black African population) and Newman (serving a predominantly mixed ancestry population) from March 2012 to July 2015. All births occurred at a single, central hospital, Paarl hospital. Thereafter, mother–infant pairs were followed at 6, 10 and 14 weeks, 6, 9 and 12 months, for healthcare and immunisations including the 13-valent pneumococcal conjugate vaccine (PCV-13) given at 6, 14 weeks and 9 months and Haemophilus influenzae type b conjugate vaccine at 6, 10, 14 weeks according to the South African Expanded Programme on Immunisation schedule [13]. Study questionnaires and clinical data were collected at enrolment and follow-up visits. A validated socioeconomic score (SES) was used to categorise participants into quartiles as lowest, low-moderate, moderate-high or highest SES [5]. Clinical data collected at each follow-up visit included details on recent respiratory tract infections, including respiratory symptoms, otitis media, wheeze or LRTIs in the preceding month and any antibiotic use in the prior 6 months. The participant’s home environment was assessed and dwellings categorised based on having two or more defined household dimensions (type of home, building material, water supply, toilet facilities, kitchen type, ventilation in kitchen areas) [5]. IAP was measured at home visits conducted antenatally (within 4 weeks of enrolment) and postnatally (between 4–6 months of the infant’s life) [5]. Home visits were conducted over 3 years with sampling occurring throughout the year covering all seasons and weather conditions. PM10 and CO were measured by separate monitors (AirChek 52; SKC, Eighty-Four, PA, USA for PM10 and Altair; Troy, MI, USA for CO) left in homes over 24 h. NO2 and VOCs, benzene and toluene, were measured using diffusion tubes (Radiello absorbent filters in polyethylene diffusive body; Sigma-Aldrich, St Louis, MO, USA) and (Markes thermal desorption tubes; Llantrisant, UK) left in homes for 2 weeks [5]. These monitors were internally calibrated for temperature and humidity as per the manufacturer information, whereas diffusion tubes were corrected for humidity during laboratory analysis [5, 14]. The South African National Ambient Air Quality Standards were used to define expected exposure levels for each pollutant based on an averaging period of 1 year for each measure [15, 16]. Maternal, paternal and household tobacco smoking and exposure were assessed using questionnaires administered at enrolment, and antenatal and postnatal visits. These were validated using maternal and infant urine cotinine measures. Maternal cotinine was measured antenatally and at birth, and infant cotinine at birth and 6–10 week with the highest result used to assign smoking status and exposure. Cotinine levels were classified as <10 ng·mL−1 (nonsmoker), 10–499 ng·mL−1 (passive smoker/exposed), or ≥500 ng·mL−1 (active smoker) [7]. Nasopharyngeal swabs were obtained from mothers (at the time of delivery) and infants at birth, 6 and 12 months by trained study staff according to World Health Organization recommendations [17]. The swabs were immediately stored in 1 mL of skimmed milk, tryptone, glucose and glycerol transport medium (STGG), transported on ice to the laboratory and frozen at −80°C for later batch processing. After thawing at room temperature (22°C), samples were vortexed for 15 s before plating out a 10 µL aliquot onto four different solid media (National Health Laboratory Services, Green Point Media Laboratory Cape Town, South Africa). Standard laboratory protocols were used for the phenotypic and biochemical identification of common bacterial species that asymptomatically colonise the upper respiratory tract. For S. pneumoniae culture, Columbia blood agar base with 2% agar, 5% horse blood and 4 mg·mL−1 gentamicin (CAG) was incubated at 37°C in 5% CO2 overnight. Presumptive S. pneumoniae isolates were identified by colony morphology, α-haemolysis, optochin disk susceptibility (Oxoid, Basingstoke, UK) and confirmed using lytA PCR [18]. For H. influenzae, bacitracin heated blood agar plates were incubated at 37°C with 5% carbon dioxide (CO2). Suspected H. influenzae colonies were inoculated onto Columbia agar and identified using Factors X, V and XV discs and by observing growth in the haemolytic zone of Staphylococcus aureus on blood agar plates. S. aureus isolates were identified by culturing on mannitol salt agar, and DNase testing whereas Moraxella catarrhalis isolates were identified by culturing on 2% blood agar and incubated overnight at 37°C. Isolates were presumptively identified by push test and confirmed by copB PCR [19]. Gram-negative bacteria were subcultured onto MacConkey agar and identified on Vitek 2® (bioMérieux, Marcy I'Etoile, France). The study was approved by the Human Research Ethics Committees of the Faculties of Health Sciences, University of Cape Town and Stellenbosch University, and by the Western Cape Provincial Health Research committee (HREC 149/2013). Mothers provided written informed consent at enrolment. Study data were captured in a relational Microsoft Access® database or collected and managed using REDCap electronic data capture tools hosted at the University of Cape Town [20]. Statistical analyses were conducted in Stata version 14.2 for Windows (Stata Corp, College Station, TX, USA). Statistical tests were considered significant if the p-value was <0.05 or if p-value cut-offs were derived using the Benjamini–Hochberg procedure for assessing the association between IAP and the pathogens [21]. Categorical variables were summarised using frequency counts and percentages, n (%). Normally and non-normally distributed continuous variables were described using mean (sd) and median (interquartile range (IQR)) values, respectively. Mann–Whitney or Wilcoxon signed-rank tests, as appropriate, were used to compare medians as well as their spread. Cross tabulations with Fishers’ exact or Chi-squared tests were used to describe and compare the prevalence of pathogen carriage between the infants (at all time points) and their mothers or between different time points for infants. Multivariable modified Poisson regression analyses with robust error variance [22] were performed to estimate adjusted risk ratios (aRRs) between each bacterial pathogen and IAP measures (individually (adjusted) or together (adjusted 2)). The association between antenatal exposures or maternal cotinine and maternal carriage was explored as was the association between postnatal exposure or infant cotinine and infant carriage. The multivariable Poisson regressions adjusted for demographic and clinical factors (weight-for-age z-score at birth, preterm, ethnicity, sex, HIV exposure, time on exclusive breastfeeding, average number of people per sleeping room, dwelling category, recent respiratory infection, day care attendance, vaccination, number of other children under 5 years in the household, antibiotic use) that have been associated with pathogen acquisition. Multivariable regressions were then further performed for each site [23, 24]. Further, we explored the possible confounding effects of bacterial co-carriage by including indicator variables for each pathogen.

Materials

N/A

Innovations

Based on the information provided, here are some potential innovations that could improve access to maternal health:

1. Mobile health clinics: Implementing mobile health clinics that can travel to peri-urban areas, where access to healthcare facilities may be limited, can provide maternal health services directly to women in need.

2. Telemedicine: Using telemedicine technology, healthcare professionals can remotely provide prenatal and postnatal care to women, reducing the need for physical visits to healthcare facilities.

3. Community health workers: Training and deploying community health workers who can provide basic maternal health services, education, and support to women in their own communities can improve access to care.

4. Health education programs: Developing and implementing health education programs that focus on maternal health, including topics such as nutrition, hygiene, and prenatal care, can empower women with knowledge to make informed decisions about their health.

5. Maternal health vouchers: Introducing voucher programs that provide financial assistance for maternal health services can help reduce the financial barriers that prevent women from accessing necessary care.

6. Public-private partnerships: Collaborating with private healthcare providers to expand access to maternal health services can help bridge the gap between supply and demand, especially in underserved areas.

7. Maternal health hotlines: Establishing toll-free hotlines staffed by trained healthcare professionals can provide women with immediate access to information, support, and guidance regarding their maternal health concerns.

8. Maternal health incentives: Implementing incentive programs, such as conditional cash transfers or maternity leave benefits, can encourage women to seek and receive regular prenatal and postnatal care.

9. Maternal health technology: Developing and utilizing innovative technologies, such as wearable devices for monitoring maternal health indicators or mobile applications for tracking prenatal care, can empower women to take an active role in managing their health.

10. Maternal health awareness campaigns: Conducting targeted awareness campaigns to educate communities about the importance of maternal health and the available services can help increase demand and utilization of maternal health services.

It’s important to note that these recommendations are based on the general need to improve access to maternal health and may not directly address the specific findings of the study mentioned.

AI Innovations Description

Based on the description provided, the recommendation to improve access to maternal health would be to implement interventions that reduce indoor air pollution (IAP) and environmental tobacco smoke (ETS) exposure during pregnancy and postnatal periods. This can be achieved through the following strategies:

1. Education and awareness: Provide pregnant women and their families with information about the harmful effects of IAP and ETS exposure on maternal and infant health. Raise awareness about the importance of creating a smoke-free environment and reducing indoor air pollution.

2. Smoking cessation support: Offer smoking cessation programs and resources to pregnant women who smoke or are exposed to secondhand smoke. Provide counseling and nicotine replacement therapy to help them quit smoking and reduce ETS exposure.

3. Indoor air quality improvement: Implement measures to improve indoor air quality in homes, particularly in low-income communities where exposure to IAP may be higher. This can include promoting proper ventilation, using clean cooking technologies, and reducing the use of solid fuels for cooking and heating.

4. Policy interventions: Advocate for and support the implementation of policies that restrict smoking in public places and promote smoke-free environments. This can help reduce exposure to ETS not only for pregnant women but also for the general population.

5. Collaboration and partnerships: Work with healthcare providers, community organizations, and government agencies to develop comprehensive strategies for addressing IAP and ETS exposure. Collaborate with local stakeholders to ensure the implementation of effective interventions and the provision of necessary resources.

By implementing these recommendations, access to maternal health can be improved by reducing the risk of respiratory infections and other health complications associated with IAP and ETS exposure. This can contribute to better maternal and infant health outcomes.

AI Innovations Methodology

Based on the information provided, here are some potential recommendations for improving access to maternal health:

1. Education and awareness campaigns: Implement programs to educate pregnant women and their families about the importance of maternal health, including the risks of indoor air pollution and tobacco smoke exposure. This can be done through community workshops, informational materials, and partnerships with local healthcare providers.

2. Improved antenatal care: Strengthen antenatal care services to include regular screenings and assessments for indoor air pollution and tobacco smoke exposure. This can help identify at-risk individuals and provide appropriate interventions and support.

3. Smoke-free environments: Advocate for smoke-free policies in homes, healthcare facilities, and public spaces to reduce exposure to environmental tobacco smoke. This can be achieved through legislation, public awareness campaigns, and support for smoking cessation programs.

4. Improved housing conditions: Address housing-related factors that contribute to indoor air pollution, such as poor ventilation and the use of solid fuels for cooking and heating. This may involve providing access to clean cooking technologies, improving housing infrastructure, and promoting sustainable energy sources.

To simulate the impact of these recommendations on improving access to maternal health, a methodology could be developed as follows:

1. Define the target population: Determine the specific population that will be impacted by the recommendations, such as pregnant women and their families in a particular region or community.

2. Collect baseline data: Gather data on the current status of access to maternal health, including rates of indoor air pollution and tobacco smoke exposure, maternal health outcomes, and healthcare utilization.

3. Develop a simulation model: Create a mathematical or computational model that simulates the impact of the recommendations on access to maternal health. This model should consider factors such as population size, demographic characteristics, healthcare infrastructure, and the effectiveness of the proposed interventions.

4. Input data and parameters: Input the collected baseline data into the simulation model, along with relevant parameters such as the expected effectiveness of the recommendations and the timeframe for implementation.

5. Run simulations: Run multiple simulations using different scenarios and assumptions to assess the potential impact of the recommendations on access to maternal health. This may involve varying factors such as the coverage of interventions, the rate of behavior change, and the availability of resources.

6. Analyze results: Analyze the results of the simulations to determine the potential outcomes of implementing the recommendations. This may include evaluating changes in maternal health outcomes, healthcare utilization, and the reduction in indoor air pollution and tobacco smoke exposure.

7. Refine and validate the model: Continuously refine and validate the simulation model based on feedback, additional data, and real-world observations. This will help improve the accuracy and reliability of the model’s predictions.

8. Communicate findings: Present the findings of the simulation study to relevant stakeholders, including policymakers, healthcare providers, and community members. This can help inform decision-making and guide the implementation of interventions to improve access to maternal health.

It is important to note that the methodology described above is a general framework and may need to be adapted based on the specific context and available data.

Authors & Co-Authors

Statistics:

Citations: 17

Authors: 8

Identifiers:

DOI: 10.1183/23120541.00052-2018

Research Areas:

Environmental, Health System and Policy, Infectious Diseases, Maternal Access, Maternal and Child Health, Quality of Care, Substance Abuse

Study Countries:

South Africa

Study Design:

Cohort Study, Cross Sectional Study

Study Approach:

Quantitative

Participants Gender:

Female