RESEARCH ARTICLE
Household Air Pollution from Solid Fuel Use
and Risk of Adverse Pregnancy Outcomes:
A Systematic Review and Meta-Analysis of
the Empirical Evidence
Adeladza K. Amegah1,2,3,5, Reginald Quansah1,6, Jouni J. K. Jaakkola1,2,3,4*
1. Center for Environmental and Respiratory Health Research, Faculty of Medicine, University of Oulu, Oulu,
Finland, 2. Public Health, Institute of Health Sciences, University of Oulu, Oulu, Finland, 3. Medical Research
Center Oulu, University of Oulu and Oulu University Hospital, Oulu, Finland, 4. Respiratory Medicine Unit,
Oulu University Hospital, Oulu, Finland, 5. Public Health, Department of Biomedical and Forensic Sciences,
University of Cape Coast, Cape Coast, Ghana, 6. School of Public Health, University of Ghana, Legon, Ghana
*Jouni.jaakkola@oulu.fi
Abstract
Background: About 41% of households globally, mainly in developing countries
OPEN ACCESS
rely on solid fuels for cooking with consequences for fetal growth and development.
Citation: Amegah AK, Quansah R, Jaakkola
JJK (2014) Household Air Pollution from Solid Fuel Previous reviews were limited in scope, assessing only two outcomes (birth weight,
Use and Risk of Adverse Pregnancy Outcomes: A stillbirth). With important evidence accumulating, there is a need to improve the
Systematic Review and Meta-Analysis of the
Empirical Evidence. PLoS ONE 9(12): e113920. previous estimates and assess additional outcomes. We conducted a systematic
doi:10.1371/journal.pone.0113920 review and meta-analysis to evaluate the quality and strength of available evidence
Editor: Tim S. Nawrot, Hasselt University, Belgium on household air pollution (HAP) and the whole range of adverse pregnancy
Received: June 15, 2014 outcomes.
Accepted: October 31, 2014 Methods: PubMed, Ovid Medline, Scopus and CINAHL were searched from their
Published: December 2, 2014 inception to the end of April 2013. All epidemiological study designs were eligible
Copyright:  2014 Amegah et al. This is an for inclusion in the review. The random-effects model was applied in computing the
open-access article distributed under the terms of summary-effect estimates (EE) and their corresponding 95% confidence interval
the Creative Commons Attribution License, which
permits unrestricted use, distribution, and repro- (CI).
duction in any medium, provided the original author
and source are credited. Results: Of 1505 studies screened, 19 studies satisfied the inclusion criteria.
Household combustion of solid fuels resulted in an 86.43 g (95% CI: 55.49, 117.37)
Data Availability: The authors confirm that all data
underlying the findings are fully available without reduction in birth weight, and a 35% (EE51.35, 95% CI: 1.23, 1.48) and 29%
restriction. All relevant data are within the paper
and its Supporting Information files. (EE51.29, 95% CI: 1.18, 1.41) increased risk of LBW and stillbirth respectively.
Funding: This work was funded by Academy of Conclusion: Combustion of solid fuels at home increases the risk of a wide range
Finland Medical Research Council grant of adverse pregnancy outcomes. Access to clean household energy solutions is the
No. 266314. The funder had no role in study
design, data collection and analysis, decision to surest way to combat HAP and mitigate their adverse effects.
publish, or preparation of the manuscript.
Competing Interests: The authors have declared
that no competing interests exist.
PLOS ONE | DOI:10.1371/journal.pone.0113920 December 2, 2014 1 / 23
Household Solid Fuel Use and Risk of Adverse Pregnancy Outcomes
Introduction
Globally, 41% of households, mainly in developing countries in Asia and sub-
Saharan Africa rely on solid fuels (coal and biomass) as their primary cooking fuel
[1]. Combustion of solid fuels in simple household cookstoves emits considerably
large amounts of health-damaging airborne pollutants including particulate
matter (PM), carbon monoxide (CO) and polycyclic aromatic hydrocarbons
(PAHs) [2] with poor ventilation of households often exacerbating the problem.
Household air pollution (HAP) from solid fuel use was attributed to 4.5 million
deaths globally in 2012, almost all in low and middle income countries [3]. There
is also strong evidence linking household solid fuel use with acute respiratory
infections in children, chronic obstructive pulmonary disease and lung cancer
later in life [4–7]. Epidemiologic evidence linking ambient air pollution exposure
with adverse pregnancy outcomes has been accumulating worldwide over the last
two decades with several studies [8–12] also attempting to summarize the
available evidence. There is however very limited evidence linking HAP exposure
from solid fuel combustion with adverse pregnancy outcomes in spite of the
widespread projection of HAP as the most important environmental exposure for
pregnant women in developing countries.
The subject matter was reviewed previously by Pope et al. [13] and Misra et al.
[14] albeit limiting the scope to only two outcomes; birth weight and stillbirth.
Both studies provided evidence of an increased risk of low birth weight (LBW)
and stillbirth with solid fuel use. Pope et al. [13] however pointed to limitations in
the extent and quality of available evidence at the time of their study. With regards
to Misra et al. [14] work, in spite of it being quite recent, it consisted of the very
same studies previously reviewed by Pope and co-workers. A recent review
proposing intervention estimates for child survival outcomes linked to HAP [15]
attempted to update the estimates of Pope and co-workers and reported only one
new eligible study on LBW with no new evidence on stillbirth found. A significant
number of important new evidence has accumulated since Pope et al. [13] review
which Bruce et al. [15] did not capture in their revised estimate. In such a rapidly
evolving area these developments call for improving the previous estimates and
assessing additional pregnancy endpoints. Also timely evaluation of methods and
results of existing studies should help inform and improve the design of future
studies. We therefore conducted a systematic review and meta-analysis of all
studies examining the relations between solid fuel use at home and pregnancy
outcomes to evaluate the quality and strength of the available evidence, and to
identify gaps in knowledge and propose future research priorities.
Methods
We conducted and report the study in accordance with the PRISMA (Preferred
Reporting Items for Systematic Reviews and Meta-Analyses) guidelines [16].
PLOS ONE | DOI:10.1371/journal.pone.0113920 December 2, 2014 2 / 23
Household Solid Fuel Use and Risk of Adverse Pregnancy Outcomes
Table 1. Search words.
Exposure Outcomes
MeSH terms Free text words MeSH terms
‘‘indoor air pollution’’ ‘‘household air pollution’’ ‘‘pregnancy outcome’’
biofuels ‘‘household fuel’’ ‘‘birth weight’’
biomass ‘‘domestic fuel’’ ‘‘low birth weight’’
coal ‘‘cooking fuel’’ ‘‘premature birth’’
wood ‘‘cooking smoke’’ ‘‘premature infant’’
charcoal ‘‘solid fuel’’ ‘‘fetal growth retardation’’
cooking firewood ‘‘fetal development’’
‘‘crop residue’’ ‘‘gestational age’’
‘‘biomass fuel’’ ‘‘small for gestational age’’
‘‘biomass smoke’’ ‘‘fetal mortality’’
‘‘wood fuel’’ ‘‘fetal death’’
‘‘wood smoke’’ ‘‘perinatal mortality’’
‘‘charcoal smoke’’ stillbirth
‘‘embryo loss’’
‘‘spontaneous abortion’’
‘‘congenital abnormalities’’
‘‘neural tube defects’’
doi:10.1371/journal.pone.0113920.t001
Search Strategy and Selection Criteria
We searched PubMed, Ovid Medline, Scopus and CINAHL from their inception
to the end of April, 2013 with no language restrictions imposed. Medical Subject
Heading (MeSH) terms and free text words were used to identify relevant studies
from the databases. The search words applied are provided in Table 1. The search
process combined the exposure and outcome terms systematically. Two
independent investigators (AKA and RQ) initially screened the articles for
eligibility based on the title and abstract. Articles were considered for inclusion if
they were (a) original studies, (b) conducted in a human population and (c)
investigated the relation between any of the exposures and outcomes listed in
Table 1. Selected articles were retrieved in full and further assessed for eligibility.
Studies were included if they either, (a) reported mean estimates for birth
measurements among exposed and unexposed groups or mean differences
between the two groups, or (b) reported effect estimates for the relation between
an exposure and an outcome, or proportion of cases of any outcome among
exposed and unexposed groups. We also reviewed the reference list of all included
studies, and the three previous reviews [13–15] to identify additional eligible
studies.
PLOS ONE | DOI:10.1371/journal.pone.0113920 December 2, 2014 3 / 23
Household Solid Fuel Use and Risk of Adverse Pregnancy Outcomes
Figure 1. Flowchart of search strategy and selection of studies for inclusion in review.
doi:10.1371/journal.pone.0113920.g001
PLOS ONE | DOI:10.1371/journal.pone.0113920 December 2, 2014 4 / 23
Household Solid Fuel Use and Risk of Adverse Pregnancy Outcomes
PLOS ONE | DOI:10.1371/journal.pone.0113920 December 2, 2014 5 / 23
Table 2. Characteristics of included studies.
Adequacy of
First author, Year Exposure confounding Quality
(Reference No.) Location Setting Design assessment Outcome control Effect estimate score
Boy, 2002 (24) Quetzaltenango Rural and urban Cross-sectional Interview. Type of BW, LBW Yes Adjusted mean differ- 6/6
Province, Western cooking fuels and ence: 63 g (95% CI:
Guatemala combustion method 0.4, 126) Unadjusted
applied (open fire or ORa: 1.21 (95% CI:
chimney stove) if 0.88, 1.66)
wood or coal was
used
Mishra, 2004 (31) Zimbabwe Nationwide Cross-sectional Interview. Main BW, LBW Yes Adjusted b: All births 5/6
household cooking 175 g (95% CI: 2300,
fuels 250), Health card
holders 120 g (95%
CI: 2301, 61),
Maternal recall 183 g
(95% CI: 2376, 10)
Unadjusted ORa: 1.12
(95% CI: 0.81, 1.54)
Mishra, 2005 (21) India Nationwide Cross-sectional Interview. Main and Stillbirth No Adjusted OR: 4/6
other types of house- Biomass fuel 1.44
hold cooking fuels, (95% CI: 1.05, 1.97),
and fuel mixing Fuel mix 1.19
ascertained. (p.0.05)
Siddiqui, 2005 (32) Sindh province, Rural and urban Prospective cohort Interview. Main cook- LBW, Stillbirth, No Adjusted OR: LBW 7/9
Southern Pakistan ing fuel used (wood, Miscarriage 1.77 (95% CI: 1.20,
NG). 2.50), Stillbirth 1.90
(95% CI: 1.10, 3.20)
Siddiqui, 2008 (25) Rehri Goth, Pakistan Semi-rural Retrospective Interview. Type of BW, LBW Yes Adjusted OR: 1.86 8/9
cohort cooking fuel (wood, (95% CI: 1.11, 3.14)
NG) at time of inter- Adjusted b: 82 g
view, during index (2170, 9)
pregnancy and any
changes since the
pregnancy. Cooking
practices and kitchen
ventilation ascer-
tained.
Tielsch, 2009 (22) Tamil Nadu, South Rural Prospective cohort Interview. Type of BW, LBW, PTB, Yes Adjusted mean differ- 8/9
India cooking fuel SGA, Stillbirth ence 104.5 g (95%
CI: 2140.1, 268.9)
Adjusted RR: LBW
1.49 (95% CI: 1.25,
1.77), PTB 1.43 (95%
CI: 1.11, 1.84), SGA
1.21 (95% CI: 1.11,
1.31), Stillbirth 1.34
(95% CI: 0.76, 2.36)
Household Solid Fuel Use and Risk of Adverse Pregnancy Outcomes
PLOS ONE | DOI:10.1371/journal.pone.0113920 December 2, 2014 6 / 23
Table 2. Cont.
Adequacy of
First author, Year Exposure confounding Quality
(Reference No.) Location Setting Design assessment Outcome control Effect estimate score
Yucra, 2011 (23) Abancay and Urban Matched case-con- Interview. Type of LBW, PTB, Yes Adjusted OR 5/9
Huancavelica trol cooking fuel, fuel Adverse perinatal (Biofuel): LBW 3.73
Districts, Peru mixing, cooking prac- outcome (LBW (95% CI: 1.14, 12.1),
tices, and kitchen and PTB com- PTB 1.59 (95% CI:
ventilation ascer- bined) 0.41, 6.18), Adverse
tained perinatal outcome
2.54 (95% CI: 1.06,
6.11) Adjusted OR
(Gas + Biofuel): LBW
1.66 (95% CI: 0.45,
5.99), Adverse peri-
natal outcome 1.40
(95% CI: 0.54, 3.60)
Thompson, 2011 Guatemala Rural Randomized con- 48-hour CO levels BW, LBW No Adjusted b: 89 g (95% 7/9
(17) trolled trial measured. Actual CI: 227, 204)
stove type (chimney Adjusted OR: 0.74
stove, open fire) used (95% CI: 0.33, 1.66)
in pregnancy ascer-
tained.
Sreeramareddy, India Nationwide Cross-sectional Interview. Main BW, LBW Yes Adjusted OR: 1.21 5/6
2011 (19) household cooking (95% CI: 1.06, 1.32)
fuels Adjusted mean differ-
ence 39.9 g (SD 13.4)
Stankovic, 2011a Nis and Niska Banja, Urban Prospective cohort Interview. Exposure to BW, Birth length No confound- Unadjusted mean dif- 6/9
(29) Serbia smoke from heating ing control but ference: BW 99.1 g
fuels (wood, coal) excluded cer- (95% CIa: 4.1, 194.1),
tain category Birth length 0 cm (p.
of mothers 0.05)
Stankovic, 2011b Nis and Niska Banja, Urban Prospective cohort Interview. Exposure to Premature labour, No confound- Unadjusted OR: 6/9
(34) Serbia smoke from heating Miscarriage ing control but Miscarriage 1.12
fuels (wood, coal) excluded cer- (95% CI: 0.70, 1.77),
tain category Premature labour
of mothers 1.07 (95% CI: 0.76,
1.52)
Abusalah, 2012 (27) Gaza Strip Urban Matched case-con- Interview. Exposure to BW, LBW Yes Adjusted Matched 6/9
trol wood fuel smoke from OR: 2.3 (95% CI: 1.2,
cooking 4.7) Adjusted b: 186 g
(95% CI: 2354, 219)
Li, 2011 (26) Shanxi Province, Rural Population-based Interview. Primary Neural tube defect Yes (in dose- Unadjusted OR: 5/9
China matched case-con- cooking and heating response ana- Cooking 1.9 (95% CI:
trol fuels, cooking and lysis). No con- 1.4, 2.6), Heating 1.7
heating practices, founding con- (95% CI: 0.2, 19.1)
kitchen location, and trol in main
housing ventilation analysis
ascertained.
Household Solid Fuel Use and Risk of Adverse Pregnancy Outcomes
PLOS ONE | DOI:10.1371/journal.pone.0113920 December 2, 2014 7 / 23
Table 2. Cont.
Adequacy of
First author, Year Exposure confounding Quality
(Reference No.) Location Setting Design assessment Outcome control Effect estimate score
Epstein, 2013 (18) India Nationwide Cross-sectional Interview. Type of pri- BW, LBW Yes Adjusted OR: 5/6
mary household fuel Biomass fuels 1.24
(95% CI: 1.04, 1.48),
Kerosene 1.51 (95%
CI: 1.08, 2.12), Coal
1.57 (95% CI: 1.03,
2.41), Solid fuelsb
1.28 (95% CI: 1.09,
1.51) Unadjusted
mean difference:
Biomass fuels 78.1 g
(95% CI: 2100.4,
55.7), Kerosene
106.5g (95% CI:
2152.5, 59.4), Coal
110 g (95% CI:
2188.5, 31.5), Solid
fuelsb 88.78 (95% CI:
225.13, 152.43)
Lakshmi, 2013 (20) India Nationwide Cross-sectional Interview. Type of Stillbirth Yes Adjusted PR: 4/6
cooking and lighting Kerosene 1.36 (95%
fuel CI: 1.10, 1.67), Wood
1.24 (95% CI: 1.08,
1.41), Other 1.23
(95% CI: 1.05, 1.44),
Solid fuelsb 1.24 (95%
CI: 1.12, 1.37)
Amegah, 2012 (28) Accra, Ghana Urban Cross-sectional Interview. Cooking BW, LBW Yes Adjusted RR: 5/6
fuel (charcoal, LPG) Charcoal 1.41 (95%
used during preg- CI: 0.62, 3.23),
nancy, fuel mixing, Charcoal & LPG 1.09
cooking practices, (95% CI: 0.41, 2.93)
kitchen ventilation, Adjusted b: Charcoal
and garbage burning 243 g (95% CI: 2496,
at home ascertained. 11), Charcoal & LPG
109 g (95% CI: 2406,
188)
Mavalankar, 1991 Ahmedabad, Western Urban Case-control Interview. Exposure to Stillbirths Yes Adjusted OR: 1.5 5/9
(33) India cooking smoke. (95% CI: 1.0, 2.1)
Mavalankar, 1992 Ahmedabad, Western Urban Case-control Interview. Exposure to Term and preterm Yes Unadjusted OR: Term 5/9
(30) India cooking smoke. LBW LBW 1.23 (95% CIa:
1.01, 1.49), Preterm
LBW 1.49 (95% CIa:
1.23, 1.81), All casesa
1.35 (95% CI: 1.15,
1.58) Adjusted esti-
mates not reported.
Household Solid Fuel Use and Risk of Adverse Pregnancy Outcomes
PLOS ONE | DOI:10.1371/journal.pone.0113920 December 2, 2014 8 / 23
Table 2. Cont.
Adequacy of
First author, Year Exposure confounding Quality
(Reference No.) Location Setting Design assessment Outcome control Effect estimate score
Samaraweera, 2010 Colombo, Sri Lanka Urban Case-control Interview. Exposure to Miscarriage No Unadjusted OR: First 5/9
(35) cooking smoke from (Trimester-speci- trimester 2.10 (95%
firewood use in a fic) CI: 0.90, 4.87).
kitchen without a Adjusted OR (Second
chimney trimester): 3.83 (95%
CI: 1.50, 9.90) All
casesa 2.54 (95% CI:
1.39, 4.63)
BW: birth weight; CI: confidence interval; CO: carbon monoxide; LBW: low birth weight; LPG: liquefied petroleum gas; OR: odds ratio; PR: prevalence ratio; PTB: preterm birth; RR: risk
ratio; SD: standard deviation; SGA: small for gestational age.
aComputed from data reported in manuscript.
bCombined estimate for the individual effect estimates reported using fixed-effects model.
doi:10.1371/journal.pone.0113920.t002
Household Solid Fuel Use and Risk of Adverse Pregnancy Outcomes
Data Extraction and Quality Assessment of Studies
Data from eligible studies were extracted independently by two investigators
(AKA and RQ) onto a form. Disagreements during synthesis of the data extracted
were resolved through discussion with the third investigator (JJKJ) serving as an
adjudicator. We contacted authors for clarifications where needed.
Methodological quality of the included studies was assessed by using the original
Newcastle-Ottawa scale (NOS, maximum of 9 stars) for case control and cohort
designs, and an adapted NOS (maximum of 6 stars) for cross-sectional designs. In
evaluating the adequacy of confounding control in the included studies, we put
together a shortlist of core confounders that needed to be adjusted for in the
analysis. The shortlist included maternal age and obstetric history, maternal
nutrition and anthropometry, socioeconomic status, and active and passive
smoking.
Statistical Analysis
We anticipated heterogeneity between the studies due to differences in study
design, and geographical settings and populations studied. We therefore applied
the random-effects model which accounts for both within and between study
heterogeneity in computing the summary-effect estimates. With regards to studies
providing multiple effect estimates (e.g. wood, coal and other solid fuels), we first
combined the effect estimates using fixed-effects model and applied the single
effect estimate in the overall meta-analysis. We quantified heterogeneity using the
Cochran Q (X2) test and the I2 statistic with a value.50% deemed to indicate
substantial heterogeneity. Forest plots were also visually assessed. We explored
possible sources of heterogeneity by conducting subgroup analysis and meta-
regression. We conducted sensitivity analysis by limiting the analysis to high
quality studies; 7 or more stars on the original NOS for case-control and cohort
studies, and 6 stars on the adapted NOS for cross-sectional studies. Publication
bias was investigated by visually inspecting funnel plots for asymmetry, and
applying the Begg’s and Egger’s tests. We accounted for publication bias using the
trim and fill method. Analyses were conducted using Stata version 9.0 (Stata
Corporation, College Station, TX, USA).
Results
A flowchart of the study selection process is depicted in Figure 1. A total of 19
studies were included in the review.
Characteristics of Included Studies
The characteristics of included studies are presented in Table 2. Seven studies
employed a cross-sectional design, of which five analyzed nationwide demo-
graphic and health survey (DHS) data. Cohort design was applied by five studies,
of which four were undertaken prospectively. One study was a randomized
PLOS ONE | DOI:10.1371/journal.pone.0113920 December 2, 2014 9 / 23
Household Solid Fuel Use and Risk of Adverse Pregnancy Outcomes
Table 3. Summary-effect estimates (EE) for the relation of solid fuel use with adverse pregnancy outcomes.
Random-effects model Heterogeneity
Outcome No. of studies EE 95% CI Cochran X2 p value I2 (%)
Birth weight 10 286.43 2117.37, 255.49 15.73 0.073 42.8
LBW 12 1.35 1.23, 1.48 15.46 0.163 28.8
Stillbirth 5 1.29 1.18, 1.41 3.73 0.443 0.0
PTB 3 1.30 1.06, 1.59 1.84 0.398 0.0
IUGR 2 1.23 1.01, 1.49 0.02 0.892 0.0
Miscarriage 2 1.65 0.74, 3.67 4.46 0.035 77.6
CI: confidence interval; EE: summary-effect estimates; IUGR: intrauterine growth retardation; LBW: low birth weight; PTB: preterm birth.
Birth weight estimate is in grams.
doi:10.1371/journal.pone.0113920.t003
controlled trial (RCT). Six studies were case-control studies of which three
adopted a matched design. Ten studies were conducted in South Asia mostly in
India with only two studies conducted in sub-Saharan Africa. Ten of the included
studies were published after the year 2010.
Figure 2. Forest plot showing the effect of household solid fuel use on birth weight (A), low birth weight (B) and Stillbirth (C). ES: effect size; CI:
confidence interval.
doi:10.1371/journal.pone.0113920.g002
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Household Solid Fuel Use and Risk of Adverse Pregnancy Outcomes
Figure 3. Funnel plot for the relation between household solid fuel use and birth weight (A), low birth weight (B) and stillbirth (C).
doi:10.1371/journal.pone.0113920.g003
With the exception of the RCT [17] exposure to HAP was assessed indirectly
through the use of questionnaires to solicit information on primary cooking and
heating fuels used by maternal households routinely or during the index
pregnancy. Thompson et al. [17] attempted to measure CO levels in households
but obtained very few measurements and as a result relied on actual stove type
(chimney stove vs. open fire) used. Six studies collected information on the use of
Table 4. Test for publication bias and adjusted summary-effect estimates.
Begg’s test Egger’s test Random-effects model
Outcome z p value Bias coefficient 95% CI p value No. of studies EE 95% CI
Birth weight 1.52 0.128 1.471 0.196, 2.746 0.029 16 253.95 286.96,
220.94
LBW 1.78 0.075 1.189 0.810, 2.297 0.038 16 1.29 1.16, 1.44
Stillbirth 0.98 0.327 1.217 20.039, 2.473 0.054 8 1.25 1.11, 1.40
CI: confidence interval; EE: summary-effect estimates; LBW: low birth weight.
Birth weight estimate is in grams.
doi:10.1371/journal.pone.0113920.t004
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Household Solid Fuel Use and Risk of Adverse Pregnancy Outcomes
Table 5. Summary-effect estimate for the relation of solid fuel use with birth weight stratified according to the study characteristics.
Random-effects model Heterogeneity
Study characteristic No. of studies EE 95% CI Cochran X2 p value I2 (%)
Geographic location
South Asia 4 274.81 2116.97, 232.65 8.65 0.034 65.3
Latin America 2 268.93 2124.10, 213.76 0.15 0.698 0.0
Sub-Saharan Africa 2 2188.30 2300.42, 276.19 0.22 0.637 0.0
Eastern Europe 1 299.1 2194.1, 24.1
Middle East 1 2186 2354, 219
Study setting
Rural 3 2100.49 2132.28, 268.69 0.25 0.882 0.0
Urban 3 2132.06 2210.65, 253.47 1.60 0.450 0.0
Study design
RCT 1 289 2204, 27
Cohort 3 2101.18 2132.41, 269.94 0.21 0.900 0.0
Case control 1 2186 2354, 219
Cross-sectional 5 275.91 2122.93, 228.88 7.49 0.112 46.6
Primary study 2 2109.38 2263.68, 44.91 1.82 0.177 45.2
Secondary analysis 3 281.22 2151.48, 210.96 5.14 0.077 61.1
Exposure assessment (Handling of solid fuel
data)
Grouped together 6 279.72 2115.21, 244.24 11.75 0.038 57.4
Separated/Specific fuels studied 4 2114.96 2177.13, 252.79 2.20 0.532 0.0
Outcome ascertainment (Place of measure-
ment)
Hospital 5 2113.71 2169.68, 257.75 2.11 0.715 0.0
Home 3 2100.49 2132.28, 268.69 0.25 0.882 0.0
Quality score
Very High 2 2101.43 2134.50, 268.35 0.21 0.647 0.0
High 2 268.93 2124.10, 213.76 0.15 0.698 0.0
Satisfactory 6 2101.56 2159.64, 243.49 10.64 0.059 53.0
CI: confidence interval; EE: summary-effect estimates.
EE are in grams.
doi:10.1371/journal.pone.0113920.t005
one specific solid fuel type with wood fuel being the most studied. Ten studies
collected information on two or more solid fuels with all the studies grouping the
individual fuels together in the assessment of HAP exposure. Six studies collected
information on kerosene use and categorized this fuel either as high pollution
[18–20] or low pollution [21–23]. Epstein et al. [18] and Lakshmi et al. [20] did
however assess their independent effects. Six studies [23–28] collected other
exposure data such as cooking habits and practices, and ventilation of cooking
area in an attempt to properly characterize exposures. Three studies [21, 23, 28]
collected information on use of combination of biomass and cleaner fuels.
Birth weight was ascertained by 14 studies and was measured at home in four
studies that were community-based [17, 22, 24, 25] within 48–72 hours using
PLOS ONE | DOI:10.1371/journal.pone.0113920 December 2, 2014 12 / 23
Household Solid Fuel Use and Risk of Adverse Pregnancy Outcomes
Table 6. Summary-effect estimate for the relation of solid fuel use with low birth weight stratified according to the study characteristics.
Random-effects model Heterogeneity
Study characteristic No. of studies EE 95% CI Cochran X2 p value I2 (%)
Geographic location
South Asia 6 1.36 1.24, 1.50 8.62 0.125 42.0
Latin America 3 1.47 0.89, 2.44 3.26 0.196 38.7
Sub-Saharan Africa 2 1.15 0.86, 1.56 0.26 0.610 0.0
Middle East 1 2.30 1.20, 4.70
Study setting
Rural 3 1.52 1.29, 1.78 0.71 0.701 0.0
Urban 4 1.66 1.14, 2.41 4.87 0.182 38.4
Study design
RCT 1 1.35 0.60, 3.03
Cohort 3 1.56 1.34, 1.82 1.16 0.559 0.0
Case control 3 1.86 1.07, 3.22 4.87 0.088 58.9
Cross-sectional 5 1.22 1.13, 1.33 0.74 0.946 0.0
Primary study 2 1.23 0.92, 1.66 0.12 0.734 0.0
Secondary analysis 3 1.22 1.12, 1.34 0.63 0.731 0.0
Exposure assessment (Handling of solid fuel data)
Grouped together 7 1.29 1.18, 1.41 8.43 0.208 28.8
Separated/Specific fuels studied 5 1.75 1.40, 2.18 1.19 0.880 0.0
Ascertainment of Outcome (Place of measurement)
Hospital 5 1.39 1.18, 1.64 5.60 0.231 28.6
Home 3 1.52 1.29, 1.78 0.71 0.701 0.0
Quality score
Very High 2 1.52 1.29, 1.80 0.63 0.428 0.0
High 3 1.42 1.10, 1.85 2.38 0.305 15.9
Satisfactory 7 1.29 1.16, 1.43 8.08 0.232 25.7
CI: confidence interval; EE: summary-effect estimates.
doi:10.1371/journal.pone.0113920.t006
infant scales. Five studies [23, 27–30] were hospital based and obtained birth
weight measures from hospital records. The studies that analyzed DHS data
[18, 19, 31] obtained birth weight measures from health cards or mother’s recall in
situations where health card was unavailable. Stillbirth was ascertained by five
studies [20–22, 32, 33] with all except the unpublished study [32] conducted in
India. Three studies [22, 23, 34] investigated preterm birth (PTB, ,37 weeks
gestation) with gestational age estimated by the last menstrual period method in
all the studies. Tielsch et al. [22] also studied SGA (newborns below the 10th
percentile of weight for gestational age at birth). Two studies [34, 35] measured
miscarriage with one study [26] ascertaining neural tube defect. Two studies
[28, 30] assessed term LBW; a proxy for intrauterine growth retardation (IUGR).
PLOS ONE | DOI:10.1371/journal.pone.0113920 December 2, 2014 13 / 23
Household Solid Fuel Use and Risk of Adverse Pregnancy Outcomes
Methodological Quality of Included Studies
Selection bias was generally minimized in all the included studies as the studies
were largely representative of their source population and reported high response
rates. Information bias was a potential problem in all the studies due to the
reliance on interview methods in assessing HAP exposure. The prospective cohort
studies collected exposure data at baseline but it is unclear whether fuel choices of
mothers remained relatively stable throughout pregnancy. The retrospective
cohort study [25], in contrast, ascertained changes in fuel type and cooking
frequency/duration during pregnancy and restricted the analysis to women who
consistently used the same fuel type during the index pregnancy. There is however
the potential for information bias due to the retrospective data collection. The
DHS surveys collected information on primary cooking fuel of households which
certainly raises doubt as to whether same fuel was used by mothers during the
index pregnancy. Of the case-control studies, only one study [27] blinded
interviewers to case/control status in the ascertainment of exposure.
Outcomes were objectively measured at home/hospital or ascertained from
hospital records for majority of the included studies. There is a strong potential
for outcome measurement bias in two studies [19, 31] which relied on maternal
recall of child size at birth to respectively estimate birth weight of 47% and 84% of
infants included in the ratio scale birth weight analysis due to unavailability of
health cards. Sreeramareddy et al. [19] further relied on maternal judgment of
baby size at birth in classifying LBW babies due to lack of birth weight data on
almost 60% of the study infants with a strong likelihood of outcome
misclassification. Epstein et al. [18] however included only newborns that had
birth weights recorded on health cards thereby excluding newborns who were not
delivered at health facilities, an approach that has obvious implications for sample
representativeness and generalizability of study findings. Of the studies that
ascertained stillbirth, only one study [21] provided a case definition in their
report. Of the two studies ascertaining miscarriage, Samaraweera and Abeysena
[35] provided a case definition whereas Stankovic et al. [34] did not. The time of
measurement of birth weight of newborns delivered at home in the community-
based studies [17, 22, 24, 25] raise doubts about their acceptability as actual birth
weight of these infants. Boy et al. [24] however excluded more remote
communities to ensure neonates were examined within 72 hours and has obvious
implications for sample representativeness and generalizability of study findings.
Tielsch et al. [22] and Thompson et al. [17] on the other hand respectively
excluded neonates not weighed within 72 hours (18.1%) and 48 hours (31.5%)
from the analysis which are also likely to bias the effect estimates.
All but two studies [29, 34] adjusted for a range of potential confounders in the
analysis including demographic, household and socioeconomic factors; maternal
nutritional, health and lifestyle factors; neonatal characteristics; and second-hand
smoke exposure. Stankovic and colleagues [29, 34] however included in their
studies only mothers who were non-smokers and reported no occupational air
pollution exposure, as well as excluding mothers with previous underlying
PLOS ONE | DOI:10.1371/journal.pone.0113920 December 2, 2014 14 / 23
Household Solid Fuel Use and Risk of Adverse Pregnancy Outcomes
Figure 4. Filled funnel plot for the relation between household solid fuel use and birth weight (A), low birth weight (B) and stillbirth (C).
doi:10.1371/journal.pone.0113920.g004
diseases (hypertension, diabetes, anemia etc.) and other present pathological
problems (infections, cervical insufficiency etc.). The studies that analyzed DHS
data and three other studies [22, 30, 33] were characterized by adjustment for
several covariates but their large sample sizes means loss of statistical efficiency
might not be a concern. Based on our a priori criteria, of the included studies that
adjusted for potential confounders, confounding control was considered
inadequate in four studies [17, 21, 32, 35].
Overall, applying the NOS scale, two studies [22, 25] were rated as very high
quality (case-control/cohort - 8 or more stars), three studies [17, 24, 32] as high
quality (case-control/cohort -7 stars; cross-sectional - 6 stars), twelve studies
[18, 19, 23, 26–29, 30, 31, 33–35] as satisfactory quality (case-control/cohort - 5 or
6 stars; cross-sectional - 5 stars) and two studies [20, 21] as low quality (,5 stars
for both case-control/cohort and cross-sectional).
Summary-Effect Estimates, Evidence of Statistical Heterogeneity
and Publication Bias
On the relation of solid fuel use with average birth weight, the study conducted in
Ghana [28] reported the highest effect size (243 g) with an Indian study [19]
PLOS ONE | DOI:10.1371/journal.pone.0113920 December 2, 2014 15 / 23
Household Solid Fuel Use and Risk of Adverse Pregnancy Outcomes
reporting the lowest effect size (39.9 g). On the relation of solid fuel use with
LBW, the study conducted in Peru [23] reported the highest and most extreme
estimate (OR53.73, 95% CI: 1.14, 12.1). The summary-effect estimate was
respectively 286.43 g (95% CI: 2117.37, 255.49) and 1.35 (95% CI: 1.23, 1.48)
for birth weight and LBW. We observed evidence of low statistical heterogeneity
in both analyses (Table 3, Figure 2). We also found evidence of publication bias in
both analyses (Figure 3) with both the Begg’s and Egger’s tests (Table 4)
confirming the funnel plot asymmetry observed. The adjusted estimates were
attenuated (Table 4). Both sensitivity analyses resulted in an increase in the
summary-effect estimate with no evidence of heterogeneity observed
(EE5292.84, 95% CI: 2121.20, 264.47, I250.0% and EE51.49, 95% CI: 1.30,
1.70, I250.0% respectively).
Regarding the other outcomes investigated, with the exception of miscarriage,
we observed no evidence of statistical heterogeneity in the analysis (Table 3). For
PTB, IUGR and stillbirth, the summary-effect estimate was 1.30 (95% CI: 1.06,
1.59), 1.23 (95% CI: 1.01, 1.49) and 1.29 (95% CI: 1.18, 1.41) respectively. The
summary-effect estimate for miscarriage (EE51.65, 95% CI: 0.74, 3.67) was
substantially elevated but not statistically significant. The small number of studies
ascertaining PTB, IUGR and miscarriage made an investigation of publication bias
impractical. Evidence of publication bias was noted in the stillbirth analysis (
Figure 3) with the adjusted estimate also attenuated (Table 4). Only one study
(26) investigated neural tube defect and reported an unadjusted OR of 1.9 (95%
CI: 1.4, 2.6) and 1.7 (95% CI: 0.2, 19.1) for cooking and heating with coal
respectively.
Sources of Heterogeneity between Included Studies
Results of the sub-group analysis which was performed for only birth weight and
LBW due to the small number of studies investigating the other outcomes are
presented in Tables 5 and 6 respectively. For birth weight, the summary-effect
estimates for the Latin American and South Asian studies were much lower than
the estimates for the Sub-Saharan African studies. The opposite was noted for the
LBW outcome. Whereas evidence of heterogeneity between the South Asian
studies was observed for both outcomes, for the Latin American studies it was
observed for only the LBW outcome. Regarding the study setting (rural vs.
urban), for both outcomes, the combined estimate for studies conducted in urban
areas was higher than the combined estimate for studies conducted in rural areas.
Also for both outcomes, the summary-effect estimates computed for studies
applying cohort design was higher than estimates summarized for studies applying
cross-sectional design. Of the cross-sectional studies, and regarding the birth
weight outcome, the summary estimate for the primary studies was higher than
the estimate computed for the studies analyzing DHS data.
Regarding information collected on solid fuel types used in households, for
both outcomes, the combined estimate recorded for studies that grouped the
various fuels together was lower than the estimate summarized for studies that
PLOS ONE | DOI:10.1371/journal.pone.0113920 December 2, 2014 16 / 23
Household Solid Fuel Use and Risk of Adverse Pregnancy Outcomes
assessed one specific fuel or investigated the fuels independently. Evidence of
heterogeneity between the studies that grouped the individual solid fuels was
noted. For the LBW outcome, the summary-effect estimates increased as the
quality of the studies increases (Table 6). An inconsistent trend was observed for
the birth weight outcome (Table 5).
In the meta-regression models; study design (cross-sectional: b520.240,
p50.022), exposure assessment (b520.342, p50.037) and study quality
(b520.160, p50.086) were the covariates associated with heterogeneity observed
in the LBW analysis. None of the covariates was statistically associated with the
observed heterogeneity in the birth weight analysis.
Discussion
Our results indicate that household use of solid fuels adversely affects pregnancy
outcomes. Solid fuel use leads to an 86.43 g (95% CI: 55.49, 117.37) reduction in
birth weight and a 35% (EE51.35, 95% CI: 1.23, 1.48) increased risk of LBW. We
also found evidence of an increased risk of stillbirth, PTB, IUGR and miscarriage
for use of solid fuel at home.
Validity of Results
Our study is based on much more information (.50%) than the previous reviews
and certainly has much higher statistical power. Some of the included studies
however had major methodological drawbacks with obvious implications for the
quality of the evidence reported. We therefore conducted sensitivity analysis by
excluding studies rated as satisfactory and low quality to assess the robustness of
our results. The summary-effect estimates from the sensitivity analyses were not
markedly different from the overall estimates. We also conducted subgroup
analysis and meta-regression to elaborate the observed heterogeneity in the
analysis. This was to ensure the inherent differences among the individual studies
that were likely to impact on the validity and usefulness of the summary estimates
are not ignored. Of the covariates explored, study design, exposure assessment
method applied, and the methodological quality appear to be the variables likely
to impact on the interpretation of our findings. For these three covariates we
observed very consistent results in the stratified analysis. The results obtained
from the meta-regression corroborated the findings from the LBW stratified
analysis.
A major validity concern of meta-analysis is the tendency of overestimating the
magnitude of the true effect size due to publication bias. We therefore investigated
publication bias and accounted for the bias where evidence of its presence was
found (Figure 4). With regards to the LBW and stillbirth outcomes, the adjusted
estimates obtained after controlling for publication bias were quite similar to the
crude estimates. Regarding the birth weight outcome, the adjusted estimate
obtained was attenuated.
PLOS ONE | DOI:10.1371/journal.pone.0113920 December 2, 2014 17 / 23
Household Solid Fuel Use and Risk of Adverse Pregnancy Outcomes
Synthesis with Previous Knowledge
We found household combustion of solid fuels to be associated with an 86 g
reduction in birth weight. Accounting for publication bias however reduced the
effect size to 54 g suggesting a possible overestimation of the summary estimate in
the meta-analysis. Pope et al. [13] previously reported a 96.6 g reduction in birth
weight for HAP exposure from solid fuel use with no evidence of publication bias
found. Our results however show that the effect estimate varies from one
population to another and also along the rural-urban divide, possibly due to the
exposure intensity which are dependent on the fuel choices. For instance, whereas
charcoal use is widespread in sub-Saharan Africa especially in urban areas, wood
which is more polluting is commonly used in South Asia. Rural African settings
patronize wood and crop residues mostly. A multi-country study reported South
Asian women to commonly use wood (49.1–89.7%), crop residue and animal
dung as domestic fuel with African women using charcoal mostly (85.4–93.5%)
[36]. Zulu and Richardson [37] also reported that more than 80% of urban
households in sub-Saharan Africa use charcoal as their main cooking fuel.
However, in the sub-group analysis, the summary estimate for studies conducted
in sub-Saharan Africa was quite larger than the estimate obtained for the South
Asian studies. Also the summary estimate computed for studies conducted in
urban settings was higher than the estimate reported for studies conducted in
rural settings. This finding could be attributed in part to the grouping together of
the individual fuels in the assessment of HAP exposure and the inconsistent
categorization of kerosene. Differences in birth weight distributions could also
partially explain the heterogeneity of effect estimates, but it should be pointed out
that an absolute effect of HAP exposure could indicate a more severe effect in a
population with lower levels of birth weight. Our finding of 35% (EE51.35, 95%
CI: 1.23, 1.48) increased risk of LBW for solid fuel use is consistent with the
findings of Pope et al. [13] study and the revised estimate by Bruce et al. [15].
We also found household use of solid fuels to be associated with a 29%
(EE51.29, 95% CI: 1.18, 1.41) increased risk of stillbirth and was quite lower than
the effect estimate previously reported by Pope et al. [13]. In addition to the four
studies reviewed by Pope and colleagues, our search strategy also identified one
other recent study [20]. This study was the largest and also reported the smallest
and most precise estimates (Combined Prevalence Ratio51.24, 95% CI: 1.12,
1.37) thereby gaining the bulk of the weight (80.41%) in the overall meta-analysis
and pulling the summary estimate towards the null as a result. This study and two
other studies [21, 33] were however excluded in the sensitivity analysis resulting in
a much higher stillbirth risk of 61% (EE51.61, 95% CI: 1.09, 2.38). It is therefore
possible the summary-effect estimate computed by our study might have been
underestimated by these large and yet low quality studies. Pope et al. [13] also
reported that their summary-effect estimate might have been underestimated by
Mishra et al. [21] study.
This is the first study to review the available evidence on household solid fuel
use and PTB, IUGR and miscarriage. Even though the findings reported are
PLOS ONE | DOI:10.1371/journal.pone.0113920 December 2, 2014 18 / 23
Household Solid Fuel Use and Risk of Adverse Pregnancy Outcomes
weakened by the small number of studies reviewed, they are consistent with the
findings of previous reviews assessing the effects of ambient air pollution [8–12]
and second-hand smoke [38, 39] on these outcomes.
Biological Plausibility
Combustion pollutants (CO, particulate matter [PM], PAH) exert their effects on
fetal growth directly by passing across the placenta or indirectly by reducing
maternal lung function and increasing the risk of maternal lung disease [9, 40].
Fetuses are highly susceptible to environmental toxicants because of their
differential exposure pattern and physiologic immaturity [41]. The high rate of
cell proliferation and changing metabolic mechanisms during the critical phase of
fetal development have been identified as the physiological process that renders
the developing fetus extremely vulnerable to environmental toxicants [42].
CO reduces oxygen-carrying capacity of maternal hemoglobin, which could
adversely affect oxygen delivery to fetal circulation [43]. CO crosses the placental
barrier [44] and with fetal hemoglobin having greater affinity for binding CO than
does adult hemoglobin [45], oxygen delivery to fetal tissues is further
compromised [46]. The resultant tissue hypoxia has the potential to reduce fetal
growth [43, 47]. Little is known about the mechanisms through which PM
exposure influences fetal growth and development. Kannan et al. [48] have
however suggested that PM exposure may cause oxidative stress, induce
pulmonary and placental inflammation, alter blood coagulation factors, influence
endothelial functions, and trigger hemodynamic responses which restrict fetal
growth through impaired transplacental oxygen and nutrient exchange.
Regarding the effects of PAHs, Dejmek et al. [49] indicated that PAHs may
directly affect early trophoblast proliferation due to their reaction with placental
growth factor receptors thereby hampering feto-placental exchange of oxygen and
nutrients, and consequently impairing fetal growth. Others have also hypothesized
that PAHs and/or their metabolites may bind to the aryl hydrocarbon receptor
resulting in antiestrogenic effects thereby disrupting the endocrine system and
interfering with uterine growth during pregnancy [50, 51]. Fetal toxicity from
DNA damage and resulting activation of apoptotic pathways have also been
proposed [52]. According to Perera et al. [41] the finding of higher DNA adduct
levels in the infant compared with the mother suggests an increased susceptibility
of the developing fetus to DNA damage.
Conclusions
Our results show that combustion of solid fuels at home increases the risk of a
wide range of adverse pregnancy outcomes. Access to clean household energy
solutions is the surest way to combat HAP and mitigate their adverse effects. This
requires political will which is often lacking in most developing countries.
PLOS ONE | DOI:10.1371/journal.pone.0113920 December 2, 2014 19 / 23
Household Solid Fuel Use and Risk of Adverse Pregnancy Outcomes
Even though we noted a high degree of consistency in study findings across the
studies reviewed, major methodological limitations of most studies means further
quality evidence are needed for causal inferences. All the studies reviewed applied
interview methods in the ascertainment of exposure with hardly any consideration
for cooking sequence and patterns, relative stability of fuel choices during
pregnancy, fuel mixing/stacking, and potency of the individual fuels in causing
adverse effects. The inconsistent categorization of kerosene is also a concern.
These observations have consequences for the validity of the results reported by
the included studies. Future research should therefore incorporate personal
exposure monitoring methods and cooking activity diaries, and evaluate
biomarkers of exposure. Other sources of HAP such as garbage burning at home
should also be explored in future studies as well as considering the relative
contribution of outdoor air pollution sources to HAP levels.
Supporting Information
Checklist S1. PRISMA Checklist.
doi:10.1371/journal.pone.0113920.s001 (DOC)
Acknowledgments
We thank Ds. Amira Simcox, University of Lausanne, Switzerland for helping with
the translation of the two Serbian studies included in the review.
Author Contributions
Conceived and designed the experiments: AA JJ. Performed the experiments: AA
RQ JJ. Analyzed the data: AA. Wrote the paper: AA RQ JJ.
References
1. Bonjour S, Adair-Rohani H, Wolf J, Bruce NG, Mehta S, et al. (2013) Solid fuel use for household
cooking: country and regional estimates for 1980–2010. Environ Health Perspect 121(7): 784–790.
2. Smith KR (2002) Indoor air pollution in developing countries: recommendations for research. Indoor Air
12: 198–207.
3. World Health Organization (WHO) (2014) Burden of disease from Household Air Pollution for 2012.
Geneva: WHO. Available: http://www.who.int/phe/health_topics/outdoorair/databases/FINAL_HAP_
AAP_BoD_24March2014.pdf. Accessed 2014 Apr 20.
4. Smith KR, Mehta S, Feuz M (2004) Indoor air pollution from household use of solid fuels. In: Ezzati M,
Rodgers A, Lopez AD, Murray, CJL, editors. Comparative quantification of health risk: Global and
regional burden of disease due to selected major risk factors. Geneva: WHO.
5. Dherani M, Pope D, Mascarenhas M, Smith KR, Weber M, et al. (2008) Indoor air pollution from
unprocessed solid fuel use and pneumonia risk in children aged under five years: a systematic review
and meta-analysis. Bull World Health Organ 86: 390–398.
6. Kurmi OP, Semple S, Simkhada P, Smith WC, Ayres JG (2010) COPD and chronic bronchitis risk of
indoor air pollution from solid fuel: a systematic review and meta-analysis. Thorax 65: 221–228.
PLOS ONE | DOI:10.1371/journal.pone.0113920 December 2, 2014 20 / 23
Household Solid Fuel Use and Risk of Adverse Pregnancy Outcomes
7. Kurmi OP, Arya PH, Lam KB, Sorahan T, Ayres JG (2012) Lung cancer risk and solid fuel smoke
exposure: a systematic review and meta-analysis. Eur Respir J 40: 1228–1237.
8. Maisonet M, Correa A, Misra D, Jaakkola JJ (2004) A review of the literature on the effects of ambient
air pollution on fetal growth. Environ Res 95: 106–115.
9. Glinianaia SV, Rankin J, Bell R, Pless-Mulloli T, Howel D (2004) Particulate air pollution and fetal
health: a systematic review of the epidemiologic evidence. Epidemiol 15: 36–45.
10. Lacasana M, Esplugues A, Ballester F (2005) Exposure to ambient air pollution and prenatal and early
childhood health effects. Eur J Epidemiol 20(2): 183–199.
11. Sapkota A, Chelikowsky AP, Nachman KE, Cohen AJ, Ritz B (2012) Exposure to particulate matter
and adverse birth outcomes: a comprehensive review and meta-analysis. Air Qual Atmos Health 5: 369–
381.
12. Stieb DM, Chen L, Eshoul M, Judek S (2012) Ambient air pollution, birth weight and preterm birth: A
systematic review and meta-analysis. Environ Res. 117: 100–111.
13. Pope DP, Mishra V, Thompson L, Siddiqui AR, Rehfuess EA, et al. (2010) Risk of low birth weight and
stillbirth associated with indoor air pollution from solid fuel use in developing countries. Epidemiol Rev
32: 70–81.
14. Misra P, Srivastava R, Krishnan A, Sreenivaas V, Pandav CS (2012) Indoor air pollution-related acute
lower respiratory infections and low birthweight: a systematic review. J Trop Pediatr 58(6): 457–466.
15. Bruce NG, Dherani MK, Das JK, Balakrishnan K, Adair-Rohani H, et al. (2013) Control of household
air pollution for child survival: estimates for intervention impacts. BMC Public Health 13(Suppl 3): S8.
16. Moher D, Liberati A, Tetzlaff J, Altman DG, The PRISMA Group (2009) Preferred Reporting Items for
Systematic Reviews and Meta-Analyses: The PRISMA Statement. PLoS Med 6(7): e1000097.
17. Thompson LM, Bruce N, Eskenazi B, Diaz A, Pope D, et al. (2011) Impact of reduced maternal
exposures to wood smoke from an introduced chimney stove on newborn birth weight in rural
Guatemala. Environ Health Perspect 119: 1489–1494.
18. Epstein MB, Bates MN, Arora NK, Balakrishnan K, Jack DW, et al. (2013) Household fuels, low birth
weight, and neonatal death in India: The separate impacts of biomass, kerosene, and coal. Int J Hyg
Environ Health 216(5): 523–532.
19. Sreeramareddy CT, Shidhaye RR, Sathiakumar N (2011) Association between biomass fuel use and
maternal report of child size at birth - an analysis of 2005–06 India Demographic Health Survey data.
BMC Public Health 11: 403.
20. Lakshmi PVM, Virdi NK, Sharma A, Tripathy JP, Smith KR, et al. (2013) Household air pollution and
stillbirths in India: Analysis of the DLHS-II National Survey. Environ Res 121: 17–22.
21. Mishra V, Retherford RD, Smith KR (2005) Cooking smoke and tobacco smoke as risk factors for
stillbirth. Int J Environ Health Res 15: 397–410.
22. Tielsch JM, Katz J, Thulasiraj RD, Coles CL, Sheeladevi S, et al. (2009) Exposure to indoor biomass
fuel and tobacco smoke and risk of adverse reproductive outcomes, mortality, respiratory morbidity and
growth among newborn infants in south India. Int J Epidemiol 38: 1351–1363.
23. Yucra S, Tapia V, Steenland K, Naeher LP, Gonzales GF (2011) Association between biofuel exposure
and adverse birth outcomes at high altitudes in Peru: a matched case-control study. Int J Occup Environ
Health 17(4): 307–313.
24. Boy E, Bruce N, Delgado H (2002) Birth weight and exposure to kitchen wood smoke during pregnancy
in Rural Guatemala. Environ Health Perspect 110: 109–114.
25. Siddiqui AR, Gold EB, Yang X, Lee K, Brown KH, et al. (2008) Prenatal exposure to wood fuel smoke
and low birth weight. Environ Health Perspect 116: 543–549.
26. Li Z, Zhang L, Ye R, Pei L, Liu J, et al. (2011) Indoor air pollution from coal combustion and the risk of
neural tube defects in a rural population in Shanxi Province, China. Am J Epidemiol 174(4): 451–458.
27. Abusalah A, Gavana M, Haidich AB, Smyrnakis E, Papadakis N, et al. (2012) Low birth weight and
prenatal exposure to indoor pollution from tobacco smoke and wood fuel smoke: a matched case-control
study in Gaza Strip. Matern Child Health J 16(8): 1718–1727.
PLOS ONE | DOI:10.1371/journal.pone.0113920 December 2, 2014 21 / 23
Household Solid Fuel Use and Risk of Adverse Pregnancy Outcomes
28. Amegah AK, Jaakkola JJ, Quansah R, Norgbe GK, Dzodzomenyo M (2012) Cooking fuel choices
and garbage burning practices as determinants of birth weight: a cross-sectional study in Accra, Ghana.
Environ Health 11(1): 78.
29. Stanković A, Mitrović V, Živadinović R (2011a) Influence of air pollution on birth weight. Srp Arh Celok
Lek 139(9–10): 651–656.
30. Mavalankar DV, Gray RH, Trivedi CR (1992) Risk factors for preterm and term low birthweight in
Ahmedabad, India. Int J Epidemiol 21(2): 263–272.
31. Mishra V, Dai X, Smith KR, Mika L (2004) Maternal exposure to biomass smoke and reduced birth
weight in Zimbabwe. Ann Epidemiol 14: 740–747.
32. Siddiqui AR, Gold EB, Brown KH, Lee K, Bhutta Z (2005) Preliminary analyses of indoor air pollution
and low birth weight (LBW) in Southern Pakistan. In: Indoor Air Pollution from solid fuels and risk of low
birth weight and stillbirth. Report from a symposium held at the Annual Conference of the International
Society for Environmental Epidemiology (ISEE), Johannesburg, South Africa, 13–16 September 2005.
Available: http://www.whqlibdoc.who.int/publications/2007/9789241505735_eng.pdf. Accessed 2013
May 5.
33. Mavalankar DV, Trivedi CR, Gray RH (1991) Levels and risk factors for perinatal mortality in
Ahmedabad, India. Bull World Health Organ 69(4): 435–442.
34. Stanković A, Mitrović V, Zivadinović R (2011) Influence of air pollution on pregnant women’s health
and pregnancy outcomes. Med Pregl 64(5–6): 279–284.
35. Samaraweera Y, Abeysena C (2010) Maternal sleep deprivation, sedentary lifestyle and cooking
smoke: Risk factors for miscarriage: A case control study. Aust N Z J Obstet Gynaecol 50(4): 352–357.
36. Kadir MM, McClure EM, Goudar SS, Garces AL, Moore J, et al. (2010) Exposure of pregnant women
to indoor air pollution: a study from nine low and middle income countries. Acta Obstet Gynecol Scand
89(4): 540–548.
37. Zulu LC, Richardson RB (2013) Charcoal, livelihoods, and poverty reduction: Evidence from sub-
Saharan Africa. Energy Sustain Dev 17(2): 127–137.
38. Salmasi G, Grady R, Jones J, McDonald SD, Knowledge Synthesis Group (2010) Environmental
tobacco smoke exposure and perinatal outcomes: a systematic review and meta-analyses. Acta Obstet
Gynecol Scand 89(4): 423–441.
39. Leonardi-Bee J, Britton J, Venn A (2011) Secondhand smoke and adverse fetal outcomes in
nonsmoking pregnant women: a meta-analysis. Pediatr 127(4): 734–741.
40. Mishra V (2004) What do we know about health effects of smoke from solid fuels combustion? East-
West Center Working Papers: Population and Health Series 117. Available: http://www.eastwestcenter.
org/sites/default/files/private/POPwp117.pdf. Accessed 2013 Sep 20.
41. Perera FP, Jedrychowski W, Rauh V, Whyatt RM (1999) Molecular epidemiologic research on the
effect of environmental pollutants on the fetus. Environ Health Perspect 107: 451–460.
42. Calabrese EJ (1986) Age and susceptibility to toxic substances. New York: Wiley & Sons.
43. Salam MT, Millstein J, Li YF, Lurmann FW, Margolis HG, et al. (2005) Birth outcomes and prenatal
exposure to ozone, carbon monoxide, and particulate matter: results from the Children’s Health Study.
Environ Health Perspect. 113(11): 1638–1644.
44. Sangalli MR, Mclean AJ, Peek MJ, Rivory LP, Le Couteur DG (2003) Carbon monoxide disposition
and permeability-surface area product in the foetal circulation of the perfused term human placenta.
Placenta 24(1): 8–11.
45. Longo LD (1977) The biological effects of carbon monoxide on the pregnant woman, fetus, and newborn
infant. Am J Obstet Gynecol 129(1): 69–103.
46. Di Cera E, Doyle ML, Morgan MS, De Cristofaro R, Landolfi R, et al. (1989) Carbon monoxide and
oxygen binding to human hemoglobin F0. Biochem 28(6): 2631–2638.
47. Bosley ARJ, Sibert JR, Newcombe RG (1981) Effects of maternal smoking on fetal growth and
nutrition. Arch Dis Child 56: 727–729.
48. Kannan S, Misra DP, Dvonch JT, Krishnakumar A (2006) Exposures to airborne particulate matter and
adverse perinatal outcomes: a biologically plausible mechanistic framework for exploring potential effect
modification by nutrition. Environ Health Perspect 114(11): 1636–1642.
PLOS ONE | DOI:10.1371/journal.pone.0113920 December 2, 2014 22 / 23
Household Solid Fuel Use and Risk of Adverse Pregnancy Outcomes
49. Dejmek J, Solanský I, Benes I, Lenı́cek J, Srám RJ (2000) The impact of polycyclic aromatic
hydrocarbons and fine particles on pregnancy outcome. Environ Health Perspect 108(12): 1159–1164.
50. Carpenter DO, Arcaro K, Spink DC (2002) Understanding the human health effects of chemical
mixtures. Environ Health Perspect 110(suppl 1): 25–42.
51. Bui QQ, Tran MB, West WL (1986) A comparative study of the reproductive effects of methadone and
benzo[a]pyrene in the pregnant and pseudopregnant rat. Toxicol 42: 195–204.
52. Nicol CJ, Harrison ML, Laposa RR, Gimelshtein IL, Wells PG (1995) A teratologic suppressor role for
p53 in benzo[a]pyrene-treated transgenic p53-deficient mice. Nat Genet 10: 181–187.
PLOS ONE | DOI:10.1371/journal.pone.0113920 December 2, 2014 23 / 23