Insecticide-Treated Nets for the Prevention of Malaria in Pregnancy: A Systematic Review of Randomised Controlled Trials

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DOI: 10.1371/journal.pmed.0040107 · Source: PubMed
Abstract
Protection from malaria with insecticide-treated bednets (ITNs) during pregnancy is widely advocated, but evidence of benefit has been inconsistent. We undertook a systematic review of randomised trials. Three cluster-randomised and two individually randomised trials met the inclusion criteria; four from Africa (n = 6,418) and one from Thailand (n = 223). In Africa, ITNs compared to no nets increased mean birth weight by 55 g (95% confidence interval [CI] 21-88), reduced low birth weight by 23% (relative risk [RR] 0.77, 95% CI 0.61-0.98), and reduced miscarriages/stillbirths by 33% (RR 0.67, 0.47-0.97) in the first few pregnancies. Placental parasitaemia was reduced by 23% in all gravidae (RR 0.77, 0.66-0.90). The effects were apparent in the cluster-randomised trials and the one individually randomised trial in Africa. The trial in Thailand, which randomised individuals to ITNs or untreated nets, showed reductions in anaemia and fetal loss in all gravidae, but not reductions in clinical malaria or low birth weight. ITNs used throughout pregnancy or from mid-pregnancy onwards have a beneficial impact on pregnancy outcome in malaria-endemic Africa in the first few pregnancies. The potential impact of ITNs in pregnant women and their newborns in malaria regions outside Africa requires further research.
Insecticide-Treated Nets for the Prevention
of Malaria in Pregnancy: A Systematic Review
of Randomised Controlled Trials
Carol Gamble
1
, Paul J. Ekwaru
2
, Paul Garner
3
, Feiko O. ter Kuile
3,4*
1 Centre for Medical Statistics and Health Evaluation, University of Liverpool, Liverpool, United Kingdom, 2 Clinical Epidemiology Unit, Makerere Medical School, Makarere
University, Kampala, Uganda, 3 Liverpool School of Tropical Medicine, Liverpool, United Kingdom, 4 Malaria Branch, Division of Parasitic Diseases, United States Centers for
Disease Control and Prevention, Atlanta, Georgia, United States of America
Funding: The authors received no
specific funding for this study.
Competing Interests: FOtK was co-
author of two of the trials reviewed.
No other conflicts of interest are
declared.
Academic Editor: Stephen J.
Rogerson, Royal Melbourne Hospital,
Australia
Citation: Gamble C, Ekwaru PJ,
Garner P, ter Kuile FO (2007)
Insecticide-treated nets for the
prevention of malaria in pregnancy:
A systematic review of randomised
controlled trials. PLoS Med 4(3):
e107. doi:10.1371/journal.pmed.
0040107
Received: June 29, 2006
Accepted: February 1, 2007
Published: March 27, 2007
Copyright: Ó 2007 Gamble et al.
This is an open-access article
distributed under the terms of the
Creative Commons Attribution
License, which permits unrestricted
use, distribution, and reproduction
in any medium, provided the
original author and source are
credited.
Abbreviations: CI, confidence
interval; EIR, entomological
inoculation rate; G[number],
gravidity [number]; Hb,
haemoglobin; HR, hazard ratio; IPT,
intermittent preventive treatment;
IPTp, intermittent preventive
treatment in pregnancy; IPTp-SP,
intermittent preventive treatment in
pregnancy with sulfadoxine-
pyrimethamine; ITN, insecticide-
treated bednet; LBW, low birth
weight; OR, odds ratio; RR, relative
risk; SP, sulfadoxine-pyrimethamine;
WHO, World Health Organization
* To whom correspondence should
be addressed. E-mail: terkuile@liv.ac.
uk
ABSTRACT
Background
Protection from malaria with insecticide-treated bednets (ITNs) during pregnancy is widely
advocated, but evidence of benefit has been inconsistent. We undertook a systematic review of
randomised trials.
Methods and Findings
Three cluster-randomised and two individually randomised trials met the inclusion criteria;
four from Africa (n ¼ 6,418) and one from Thailand (n ¼ 223). In Africa, ITNs compared to no nets
increased mean birth weight by 55 g (95% confidence interval [CI] 21–88), reduced low birth
weight by 23% (relative risk [RR] 0.77, 95% CI 0.61–0.98), and reduced miscarriages/stillbirths by
33% (RR 0.67, 0.47–0.97) in the first few pregnancies. Placental parasitaemia was reduced by
23% in all gravidae (RR 0.77, 0.66–0.90). The effects were apparent in the cluster-randomised
trials and the one individually randomised trial in Africa. The trial in Thailand, which randomised
individuals to ITNs or untreated nets, showed reductions in anaemia and fetal loss in all
gravidae, but not reductions in clinical malaria or low birth weight.
Conclusions
ITNs used throughout pregnancy or from mid-pregnancy onwards have a beneficial impact
on pregnancy outcome in malaria-endemic Africa in the first few pregnancies. The potential
impact of ITNs in pregnant women and their newborns in malaria regions outside Africa
requires further research.
The Editors’ Summary of this article follows the references.
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P
L
o
S
MEDICINE
Introduction
Approximately 50 million pregnant women are exposed to
malaria each year. Pregnant women are more susceptible to
malaria, placing both mother and fetus at risk of the adverse
consequences [1–3]. In areas of low and unstable trans-
mission, such as in many regions in Asia and the Americas,
women do not acquire substantial antimalarial immunity, and
are susceptible to episodes of acute and sometimes severe
malaria, and fetal and maternal death [4]. In areas with stable
malaria transmission, such as in most of sub-Saharan Africa,
infection with Plasmodium falciparum in pregnancy is charac-
terised by predominantly low-grade, sometimes sub-patent,
persistent or recurrent parasitaemia. These infections fre-
quently do not result in acute symptoms yet are a substantial
cause of severe maternal anaemia [5] and of low birth weight
(LBW) [3], and as such are a potential indirect cause of early
infant mortality [6–8]. Because most of these infections
remain asymptomatic, and therefore undetected and un-
treated, prevention of malaria in pregnancy is especially
important in these settings.
The World Health Organization (WHO) advocates a three-
pronged approach to malaria control in pregnancy that
includes the use of insecticide-treated bednets (ITNs),
intermittent preventive treatment (IPT), and case manage-
ment (treatment) [9]. In areas of stable malaria transmission
in sub-Saharan Africa, ITNs are highly effective in reducing
childhood mortality and morbidity from malaria [10].
Although ITNs are promoted as a major tool in the fight
against malaria in pregnancy, the available evidence about
their efficacy in pregnancy has been inconsistent. In this
review, we summarise the available data from randomised
controlled trials that compared the effects of ITNs to no nets,
or to untreated nets, on the health of pregnant women and
birth outcome.
Methods
A protocol was developed for this review [11], and the
standard search strategy of the Cochrane Infectious Diseases
Group was used to identify potentially relevant trials [12]. The
inclusion criteria were all trials that randomised individuals
(pregnant women) or clusters (community or antenatal
clinics) in areas where malaria transmission occurs. Where
cluster-randomised trials were identified, the methods of
analysis were checked to ensure that the precision of the data
extracted from the reports was correctly estimated. The
authors needed to have adjusted for clustering, as ignoring
the clustering provides the correct point estimate of the
magnitude of the trial effect but may overestimate the
precision, resulting in potentially incorrect conclusions [13].
Primary outcomes selected were mean haemoglobin and
anaemia, and mean birthweight and LBW; secondary out-
comes included peripheral malaria in the mother assessed by
finger prick during pregnancy or at birth, placental malaria
assessed by microscopy, clinical malaria, pre-term birth, fetal
loss (defined as miscarriage or stillbirth), and maternal death.
Trial quality was assessed as adequate, inadequate, or
unclear based on the methods used to generate the allocation
sequence and allocation concealment [14]. Minimisation of
loss to follow-up was considered adequate (90% of the
participants randomised included in the analysis), inadequate
(, 90%), or unclear (not reported).
Outcomes were combined using the inverse variance
method in RevMan [15,16]. We used the fixed-effects model
throughout, and assessed heterogeneity by the I
2
test (with
values of .50% representing moderate heterogeneity) [17].
To minimise the anticipated heterogeneity, no attempt was
made to combine trials that compared ITNs to no nets and
those that compared ITNs to untreated nets [10]. Because all
the included studies from Africa compared ITNs to no nets,
and the one study comparing ITNs to untreated net was
conducted in Thailand, this also resulted in stratification by
the major malaria transmission regions (Africa versus non-
Africa), which differ in transmission intensity, p arasite
species, predominant vector, and vector behaviour.
The effect of ITNs was expected to be greatest in the first
few pregnancies because women develop pregnancy-specific
immunity against placental parasites over successive preg-
nancies as a consequence of repeated exposure [18]. Because
gravidity was considered the greatest potential modifier of
the effect of ITNs, analyses were stratified a priori by
gravidity groups whenever this was possible based on the
details provided.
Other potential sources of effect modifications that were
explored included concomitant use of IPT in pregnancy
(IPTp), and differences between trials that used individual
randomisation, in which women bene fit primarily from
personal protection by treated nets, and trials that used
cluster randomisation. In the latter trials, ITNs were
distributed to whole communities, which may result in a
mass or community effect due to area-wide killing of the
malaria-transmitting mosquitoes [19–21]. Women i n the
cluster-randomised trials were mostly provided with ITNs
prior to becoming pregnant and were thus pr otected
throughout pregnancy. In the individually randomised trials,
nets were provided as part of antenatal care, i.e., typically
from 20 to 24 wk onwards. We could not explore other
potential sources of heterogeneity because the number of
trials identified was too few.
Results
Description of Trials
Six trials were identified; we excluded one trial as the
analysis had not adjusted for clustering, and loss to follow-up
was high (Text S1) [22]. Of the five included trials (Table 1),
two were individually randomised [23,24], and three were
cluster-randomised with analysis that took design effects into
account [25–27].
Four trials were conducted in stable malaria-endemic areas
in Africa (three in Kenya [24,26,27] and one in northern
Search Strategy and Selection Criteria
Data for this review were identified by searches of the electronic
databases in Medline, PubMed, EMBASE, and LILACS, using the search
terms ‘‘ malaria’’ , ‘‘ pregnan*’’ ,(‘‘ women’’ OR ‘‘ woman’’ ) ‘‘ net*’’ , ‘‘ ITN*’’,
and ‘‘ ITM*’’ . We also searched the Cochrane Infectious Diseases Group’s
trials register, and the Cochrane Central Register of Controlled Trials
(CENTRAL), published in The Cochrane Library (Issue X, 2005). We also
reviewed the reference lists of all trials identified by the above methods.
Unpublished information was solicited from individual researchers and
organisations working in the field. There were no restrictions on year or
language of publication.
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Insecticide-Treated Nets in Pregnancy
Table 1. Characteristics of Included Studies
Trial Country Year of
Study
Type of
Trial
Quality Comparison Insecticide
a
IPTp
Policy
Participants Transmission Notes
Unit of
Random-
isation
Sequence
Generation
Concealment
of Allocation
Inclusion of
Participants
Gravidity N
Dolan
et al. [23]
Thailand 1990–1992 Individual Antenatal
clinic
attendee
Not described Not described Adequate ITNs vs.
untreated
nets
b
Permethrin None All 341 Low unstable
transmission;
P. falciparum and
P. vivax; EIR 0.5/y
No-net
group
excluded
b
Njagi et al.
[24,29]
Kenya 1997–1999 Individual Antenatal
clinic
attendee
Adequate Not described Inadequate
for delivery
outcome
ITNs vs.
no nets
c
Cyfluthrin IPTp
randomised
c
G1
and G2
963 Intense perennial;
P. falciparum;
EIR 60–300/y
Factorial
design
c
Browne
et al. [25]
Ghana 1994–1995 Cluster Village (98) Adequate Adequate Inadequate
for delivery
outcome
ITNs vs.
no nets
Permethrin None All 1,961 Hyperendemic, perennial
with marked seasonal
variation; P. falciparum;
EIR 100–300/y
Part of ITN
child mortality
trial
Shulman
et al. [26]
Kenya 1994–1995 Cluster Zone (56) Adequate Adequate Adequate for
third trimester
blood and for
follow-up .4
wk after delivery
ITNs vs.
no nets
Permethrin None G1 503 Perennial with marked
seasonal variation;
P. falciparum; EIR 10/y
Part of ITN
child mortality
trial
ter Kuile
et al. [27]
Kenya 1997–1999 Cluster Village (79) Adequate Adequate Adequate ITNs vs.
no nets
Permethrin None All 2,991 Intense perennial;
P. falciparum;
EIR 60–300/y
Part of ITN
child mortality
trial
a
Permethrin at 500 g/m
2
.
b
No-net group excluded from analysis because this group received untreated nets from a local non-governmental aid organisation during the study.
c
Factorial design ITNs versus no nets and IPTp-SP versus placebo.
doi:10.1371/journal.pmed.0040107.t001
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Insecticide-Treated Nets in Pregnancy
Ghana [25]), all with entomological inoculation rate (EIR) . 1/
y, and one in Karen refugee camps along the Thailand–
Myanmar border in an area with low and markedly seasonal
malaria where P. falciparum and P. vivax coexist (EIR 0.5/y) [23].
The African trials compared ITNs to no nets; 6,418 women
were enrolled [24–27]. The remaining trial from Thailand
randomised individual women to receive either ITNs, un-
treated nets, or no nets [23]. In the ‘‘ no nets’’ arm, a large
proportion of women received nets from another donor
independent of the study, and the researchers split the results
in this control arm into women using donor nets and women
not using donor nets. Because this compromised the validity
of the control arm, we included only the comparison of ITNs
with untreated nets (n ¼ 223).
All African trials gave double- or family-sized nets to each
household. The nets used in Thailand were smaller single-
sized nets (70 3 180 3 150 cm). All trials used the widely
available insecticide permethrin (500 g/m
2
), except one trial
that used cyfluthrin [24].
One trial included IPTp-SP in a factorial design [24].
Women were allocated to receive (1) ITNs plus IPTp-SP, (2)
IPTp-SP alone, (3) ITNs plus IPTp-SP placebo, or (4) IPTp-SP
placebo alone (‘‘ control’’ ). None of the other trials included
IPT.
In the four trials from Africa, only women having their first
baby were included in one trial [26], women having their first
or second baby in another [24], and women of all gravidity in
the remaining two trials (Table 1) [25,27]. In the trials
includin g pregnant women of all gravidity, the authors
analysed them dif ferently: ter Kuile et al. grouped by
gravidity 1 to 4 (G1–G4) and gravidity 5 and above (G5þ)
[27]. Browne et al. grouped by first pregnancy (G1), second
pregnancy (G2), and third pregnancy and above (G3þ) for
continuous endpoints [25]. To allow for sub-group analysis by
gravidity group, we grouped the G3þ group from Browne et
al. and the G5þ group from ter Kuile et al. into one sub-
group, referred to as ‘‘ high gravidity’’ , and the G1 from
Shulman et al., the G1 and G2 groups from Browne et al. and
Figure 1. Effect of ITNs versus No Nets in Africa on Mean Haemoglobin Levels (in Grams/Litre)
The red squares represent the effect estimates of ITNs; the black lines represent the 95% confidence intervals associated with the effect estimates (a line
with an arrow indicates that the confidence interval was greater than could be illustrated in the graph). The black diamonds represent the summary
effect estimates for the different subgroups (‘‘ subtotal’’ ) and for the overall effect (‘‘ total’’ ). ‘‘ Dry’’ and ‘‘ wet’’ refer to the dry and wet seasons. SPþ,
women randomized to IPTp-SP; SP-, women randomized to receive placebo ITPp (factorial design).
doi:10.1371/journal.pmed.0040107.g001
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Insecticide-Treated Nets in Pregnancy
the G1–G4 group from ter Kuile et al. into another sub-
group, referred to as ‘‘ low gravidity’’ [25–27]. The study by
Browne et al. also provided sub-group analyses for dichot-
omous endpoints, but unlike in the analysis for continuous
endpoints they were not adjusted for cluster randomisation
[25].The study by Dolan et al. in Asia did not provide
estimates by gravidity group, with the exception of the effect
on birth weight [23].
Treated Nets versus No Nets (Four Trials in Africa)
Primary outcomes. All four trials reported the effect of
ITNs on haemoglobin (Hb) levels and anaemia. Because of
the variations in trial design and reporting, it was not
possible to combine the results from all four trials for
anaemia (Hb , 100 or 110 g/l) and severe anaemia (Hb , 70
or 80 g/l) [28]. The results for mean haemoglobin are
provided by the time of assessment (third trimester or
delivery) and by gravidity group (Figure 1).
There was no evidence for improved haemoglobin levels in
women having their first or second babies in the two trials
that assessed haemoglobin levels in the third trimester
[25,26]. The overall (i.e., all gravidae) summary odds ratio
(OR) for any anaemia in the third trimester was 0.88 (95%
confidence interval [CI] 0.71–1.10, p ¼ 0.26, one trial) and for
severe anaemia was 0.77 (0.56–1.08, p ¼ 0.13, two trials).
Insufficient details were reported to provide sub-group
analysis by gravidity group.
There was significant heterogeneity of treatment effect
between the two other trials and sub-groups that assessed
haemoglobin levels at delivery, with no evidence for a
consistent effect overall (Figure 1) [24,27]. Mean haemoglo-
bin levels were significantly higher in G1–G4 in the trial by
ter Kuile et al., who also reported a significant delay in the
time to the first episode of any anaemia (Hb , 110 g/l) in G1–
G4 (hazard ratio [HR] 0.79, 95% CI 0.65–0.96, p ¼ 0.02), but
not in G5þ (HR 1.00, 0.86–1.18, p ¼ 0.97) [27]. Njagi et al. did
not find a significant increase in the mean haemoglobin
levels of primi- and secundigravidae (Figure 1) or a
significant overall reduction in any anaemia, although sub-
group a nalysis by gravidity showed that a significant
reduction in any anaemia was found in primigravidae and
not secundigravidae (not shown) [29].
All four trials comparing nets to no nets reported on mean
birth weight (Table 2; Figure 2). The average birth weight was
55 g higher in the ITN group in women of low gravidity, but
no difference was detected in women of higher gravidity
groups. For LBW, two trials contributed (Table 2), indicating
women of low gravidity had a 23% reduction in LBW, but
there was no apparent effect in women of high gravidity in
the one trial measuring this [27]. There was also no evidence
for an effect in women receiving IPTp with sulfadoxine-
pyrimethamine (IPTp-SP) (one trial) (Figure 2). Browne
reported the overall OR adjusted for clustering for all
gravidity as 0.87 (95% CI 0.63–1.19); as no information was
provided by gravidity group, and because LBW was a
common event in this trial, the OR could not be pooled
with the relative risk (RR) estimates from the other trials.
Secondary outcomes. All four RCTs reported on malaria
parasitaemia. One trial tested women every month and
showed time to first infection in the ITN group was reduced
(HR 0.67, 95% CI 0.52–0.86, p ¼ 0.002) [27]. The prevalence of
parasitaemia was less common in the ITN groups when
Table 2. Summary Effect Measures of Four Trials Comparing ITNs versus No Nets in Africa
Endpoint
Type
Measure Number
of Trials
Measure
a
All Gravidae Low Gravidity
b
High Gravidity
b
Trials Effect
a
95% CI p-Value Trials Effect
a
95% CI p-Value Trials Effect
a
95% CI p-Value
Continuous Haemoglobin (g/l)
c,d
4 Diff [25–27,29] 0.5 1.0 to 2.0 0.50 [25–27,29] 0.6 1.2 to 2.3 0.52 [25,27] 0.3 2.3 to 3.0 0.80
Birth weight (grams)
c
4 Diff [24–27] 33 5 to 62 0.02 [24–27] 55 21 to 88 0.001 [25,27] 20 74 to 33 0.45
Dichotomous LBW (,2,500 g)
c
2 RR [24,27] 0.80 0.64 to 1.00 0.05 [24,27] 0.77 0.61 to 0.98 0.03 [27] 1.12 0.56 to 2.24 0.75
Placental malaria
(microscopy)
3 RR [24,26,27] 0.77 0.66 to 0.90 0.0009 [24,26,27] 0.78 0.66 to 0.92 0.003 [27] 0.72 0.48 to 1.08 0.12
Pre-term delivery
(,37 wk)
1 RR [27] 0.74 0.42 to 1.31 0.30 [27] 0.66 0.34 to 129 0.22 [27] 1.02 0.33 to 3.15 0.97
Fetal loss
(miscarriage/stillbirth)
3 RR [24,26,27] 0.68 0.48 to 0.98 0.04 [24,26,27] 0.67 0.47 to 0.97 0.03 [27] 1.02 0.17 to 6.23 0.98
a
Effect measure obtained from fixed effect models. Diff, mean difference.
b
Low gravidity indicates women of gravidity 1 or 2 (from [24–26, 29]) or 1–4 (from [27]); high gravidity indicates women of gravidity 3þ (from [25]) or 5þ (from [27]).
c
Primary outcome.
d
Haemoglobin levels during the third trimester or at the time of birth.
Browne et al. [25] provided sub-group analysis that was adjusted for the cluster design for continuous endpoints (birth weight, haemoglobin, and parasite densities) by primi- (G1), secundi- (G2), and multigravidae (G3þ), but not for any of the
dichotomised outcomes. Although proportions by gravidity group were provided, cluster-adjusted estimates of the precision of effect were available only for the overall effect and not by gravidity group.
doi:10.1371/journal.pmed.0040107.t002
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Insecticide-Treated Nets in Pregnancy
assessed in the third trimester (OR 0.88, 073–1.06, p ¼ 0.19,
two trials) [25,26] or at the time of delivery (RR 0.76, 0.67–
0.86, p , 0.001, two trials) [24,27]. Placental malaria para-
sitaemia was lower with ITNs by 23% (95% CI 10–34, three
trials; Table 2). There was no evidence for an effect on the
prevalence of peripheral or placental malaria in women who
were provided IPTp-SP (one trial, Figure 3) [24].
Geometric mean parasite densities in peripheral blood
tended to be lower in the ITN groups in women having their
first or second baby, although the result was not statistically
significant (geometric mean ratio 0.82, 95% CI 0.66–1.02, p ¼
0.07, two trials) [24,25]. There was no evidence for a beneficial
effect in G3þ in the trial by Browne et al. (geometric mean
ratio 1.28, 0.90–1.82, p ¼ 0.17). Ter Kuile reported that
maternal and placental parasite densities were identical in
parasitaemic women from ITN and control villages, but
insufficient details were provided for inclusion in this analysis
[27].
Clinical malaria was reported in two trials, and episodes
were less frequent in the ITN than in the control groups in
both trials, but this was not significant. Shulman et al.
reported on self-reported illness with parasitaemia (OR 0.85,
95% CI 0.47–1.54) [26], and ter Kuile et al. reported on any
documented parasitaemia with documented fever based on
monthly assessments in G1–G4 (HR 0.72, 95% CI 0.19–2.78)
[27].
No effect was demonstrated in the one trial measuring pre-
term delivery (,37 wk of gestation) [27] (Table 2).
The three trials reporting on fetal loss (miscarriage or
stillbirth) showed a consistent reduction in fetal loss
associated with ITNs in low gravidity women (33%, 95% CI
3–53, p ¼ 0.03; Figure 4; Table 2). Browne et al. [25] did not
provide a breakdown by intervention group.
Maternal death was reported by Njagi [24] (five deaths),
with no trends evident by group; Shulman et al. [26] reported
four deaths but did not specify the groups.
ITNs versus Untreated Nets (One Trial from Thailand)
This trial was conducted on the Thailand–Myanmar
border, with individual randomisation [23]. Fewer women
experienced peripheral malaria parasitaemia in the ITN
group, but this was not significant (RR 0.73, 95% CI 0.47–
1.04); however, in women infected with malaria, the geo-
metric mean parasite density was lower in the ITN group (507
versus 1,096, p ¼ 0.049), and anaemia (hematocrit , 30%) was
less frequent with ITNs (RR 0.63, 95% CI 0.42–0.93). Mean
birth weight was similar between the two groups (ITN group,
2,858 g, standard deviation 486, n ¼ 94, versus untreated net
group, 2,891 g, standard deviation 481, n ¼ 85), as was LBW
(RR 1.04, 95% CI 0.52–2.07) and pre-term delivery (RR 0.92,
95% CI 0.45–1.88). Fetal loss was significantly lower in the
ITN group (2/102, 2%) than the untreated net group (10/97,
10%) (RR 0.21, 95% CI 0.05–0.92). The number of maternal
deaths was similar (ITN group, 0/103, versus untreated net
group, 2/100).
Figure 2. Effect of ITNs versus No Nets in Africa on Mean Birth Weight (in Grams)
The red squares represent the effect estimates of ITNs; the black lines represent the 95% confidence intervals associated with the effect estimates. The
black diamonds represent the summary effect estimates for the different subgroups (‘‘ subtotal’’) and for the overall effect (‘‘ total’’ ). ‘‘ Dry’’ and ‘‘ wet’’
refer to the dry and wet seasons. SPþ, women randomized to IPTp-SP; SP-, women randomized to receive placebo ITPp (factorial design).
doi:10.1371/journal.pmed.0040107.g002
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Insecticide-Treated Nets in Pregnancy
Discussion
This systematic review shows that ITNs were associated with
some important health benefits for pregnant women and their
babies. Women of low gravidity randomised to ITNs delivered
fewer LBW babies and were less likely to experience fetal loss
(miscarriage or stillbirth). Although the latter was not a
primary endpoint in the trials, it is an important outcome. No
significant decrease was observed in pre-term deliveries in the
single trial that assessed this outcome. The consistent
reduction observed in the miscarriage and stillbirth rates
suggests that the attributable effect of malaria on fetal loss
may be underestimated in malaria-endemic Africa, where
most women remain asymptomatic when infected with P.
falciparum. Despite the reduction in malaria infections, no
overall effect on mean haemoglobin was demonstrated, and
data on maternal anaemia were inconsistent.
WHO currently recommends that women in malaria-
endemic areas of Africa use both IPTp-SP and ITNs in
pregnancy to prevent malaria. One of the two trials from
western Kenya assessed the effect of ITNs and IPTp-SP
simultaneously, using a factorial design. This trial showed that
ITNs provided benefits in primigravidae when used alone, but
it did not demonstrate additional benefits of the combined
interventions over either of the single interventions [24,29].
The main benefit of ITNs in women protected by IPTp-SP
may thus occur after birth through protection of infants from
malaria, since infants typically share sleeping space with the
mother for the first several months to years [30]. Similar
considerations apply to the benefit of ITNs in grand-multi-
gravidae (G5þ), as no direct beneficial effect on the develop-
ing fetus in terms of birth weight or fetal loss was apparent in
this group.
The only trial included in this analysis that compared ITNs
to untreated nets was also the only trial conducted outside of
Africa, in an area with highly seasonal P. falciparum and P.
vivax malaria on the Thailand–Myanmar border. It showed a
statistically significant reduction in anaemia and fetal loss in
all gravidae, but no evidence for a beneficial effect on birth
weight or gestational age [23].
Extrapolation of results from the three cluster-randomised
trials to predict the potential impact of programmes that
distribute ITNs to individual pregnant women as part of
antenatal care should be done with caution. Firstly, nets
distributed as part of antenatal care will leave most women
exposed to malaria in the first third or half of pregnancy,
when the risk of peripheral malaria parasitaemia is greatest
[3]. By contrast, most women in the cluster-randomised trials
became pregnant after ITNs were distributed and were as such
protected throughout pregnancy. Secondly, the effect of ITNs
in the cluster-randomised trials reflects the combined effects
of personal protection (individual barrier protection) and
area-wide reductions in malaria transmission (community or
mass effect) [19–21]. It is possible that the mass killing effect
on mosquito populations in areas with a high ITN coverage
will result in stronger treatment effects of ITNs than can be
achieved with ind ividual ne ts. It is also likely tha t the
community effect in the cluster-randomised trials resulted
in a slight underestimation of the magnitude of the effect of
Figure 3. Effect ITNs versus No Nets in Africa on Placental Malaria
The red squares represent the effect estimates of ITNs; the black lines represent the 95% confidence intervals associated with the effect estimates (a line
with an arrow indicates that the confidence interval was greater than could be illustrated in the graph). The black diamonds represent the summary
effect estimates for the different subgroups (‘‘ subtotal’’ ) and for the overall effect (‘‘ total’’ ).
Placental malaria was defined as the presence of asexual parasitaemia detectable by microscopy. Data from Shulman et al. [26] are based on 25.8% of all
enrolled women, and includes only women who delivered in the hospital. The degree of heterogeneity approached moderate levels (I
2
¼ 49.9%) in the
low gravidity group. Similar analysis using random instead of fixed-effect models gave a summary effect of 0.82 (0.61–1.11), 0.72 (0.48–1.08), and 0.79
(0.63–0.98) for low, high, and all gravidae, respectively. SPþ, women randomized to IPTp-SP; SP-, women randomized to receive placebo ITPp (factorial
design).
doi:10.1371/journal.pmed.0040107.g003
PLoS Medicine | www.plosmedicine.org March 2007 | Volume 4 | Issue 3 | e1070512
Insecticide-Treated Nets in Pregnancy
ITNs because women living in control ho useholds fr om
adjacent villages not using ITNs will have benefited from the
area-wide reductions in vector populations, as has been shown
for effect estimates in young children [19]. Similar consid-
erations apply to the trial comparing ITNs with untreated nets
from the Thailand–Myanmar border [23]. Although, this trial
randomised individual women, all trial participants lived in
the same densely populated refugee camps and some mass
effect by the treated nets cannot be excluded.
The most recent trial from western Kenya by Njagi et al. is
informative in this respect, as it is the only trial that compared
the effects of ITNs versus no nets using simple randomisation
by individual in an area with low ITN coverage (little or no
mass effect) [24,29]. This trial and the community-randomised
trial by ter Kuile et al. [27] were conducted simultaneously in
contiguous areas with similar malaria transmission at baseline,
and similar socioeconomic and educational s tatus and
ethnicity of the trial population. The effect estimates were
similar between the two trials (in women not randomised to
IPTp-SP), suggesting that ITNs may work equally well when
provided to individuals as part of antenatal care in the second
trimester or when provided to entire communities.
The systematic review was informative, but there were
some limitations stemming from the variety in trial designs
and the number of trials. Outcome data were often expressed
in different ways, and inclusion or analysis of gravidity groups
was different. How anaemia and peripheral parasitaemia
were detected and treated varied, with different periods of
follow-up and di fferent cut-offs, limiting our ability to
provide summary estimates for some of the endpoints, or to
provide sub-group analysis by gravidity group where desired.
Shulman et al. and Njagi et al. tested and treated women only
if they were suspected of being anaemic or of having malaria,
but Dolan et al. performed weekly blood tests, and ter Kuile
et al. tested monthly. The number of studies included in the
analysis was limited. All four African studies were conducted
in areas with stable malaria transmission with EIRs ranging
from 10/y to 300/y. Three of the four were conducted in
Kenya, and two of these in adjacent areas with similarly
intense perennial transmission. These two studies had the
greatest influence (expressed as the weight in the figures) on
the overall results of the systematic review, particularly for
the effect on placental malaria because in the trial by
Shulman et al. [26] data were available for only 25.8% of
women (those that delivered in the hospital). It is plausible
that the 25.8% were different to those delivering at home and
may not be representative of all those randomised. This may
also explain some of the observed heterogeneity of the effect
of ITNs on placental malaria.
Although relatively few trials have been conducted and
some questions on the efficacy of ITNs in pregnant women in
Africa remain, the four trials comparing ITNs with no nets
suggest significant beneficial effects of ITNs on birth weight
and fetal loss in the first few pregnancies in areas with
moderate to intense malaria transmission in sub-Saharan
Africa. These findings are consistent with a non-randomised
trial of the effect of socially marketed ITNs conducted in an
area with intense perennial malaria transmission in southern
Tanzania [31], and with an excluded randomised controlled
trial from The Gambia, which has lower and highly seasonal
transmission [22]. These observed beneficial effects of ITNs
during the first few pregnancies, together with the absence of
Figure 4. Effect of ITNs versus No Nets in Africa on Miscarriage or Stillbirth
The red squares represent the effect estimates of ITNs; the black lines represent the 95% confidence intervals associated with the effect estimates (a line
with an arrow indicates that the confidence interval was greater than could be illustrated in the graph). The black diamonds represent the summary
effect estimates for the different subgroups (‘‘ subtotal’’ ) and for the overall effect (‘‘ total’’ ).
Data from Shulman et al. [26] refer to stillbirths only. As the event is rare (,10%), the OR reported by Shulman et al. approximates an RR and has been
combined with the RRs of Njagi [24] and ter Kuile et al. [27]. SPþ, women randomized to IPTp-SP; SP-, women randomized to receive placebo ITPp
(factorial design).
doi:10.1371/journal.pmed.0040107.g004
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Insecticide-Treated Nets in Pregnancy
apparent harm to the developing fetus, the potential
beneficial effect on the infant when the net continues to be
used after birth [10], and the potential for ITNs to reduce
malaria transmission through a mass killing effect on
mosquito populations, support the current recommendations
from WHO to provide ITNs for pregnant women in all
regions with stable malaria transmission throughout sub-
Saharan Africa, regardless of the degree of malaria trans-
mission intensity.
Further evaluation of the potential effect of ITNs on
pregnant women and their infants is warranted in malaria
regions including the Americas, Asia, and the southwest
Pacific, which represent approximately half of all pregnant
women exposed annually to malaria. The more complex
vector populations with exophagic, exophilic, and early biting
behaviour in some of these areas may result in lower efficacy
of ITNs than in Africa, where Anopheles gambiae s.s. is the most
important vector. These studies should include women of all
gravidae, and ideally address the interaction between ITNs
and drug-based prevention such as IPTp, which is also largely
untested outside of Africa. In Africa, it took over a decade for
the evidence of ITN or IPTp efficacy in pregnant women to
accumulate. It would be more efficient if trials had a common
design, and if systematic reviews used individual patient data
to allow appro priate collection of design effects, more
accurate and standardised handling of the data, and more
robust sub-group analysis. In order to enhance the rate at
which evidence becomes available and is translated into
policy, future trials would clearly benefit from better co-
ordination between research groups.
Supporting Information
Text S1. QUOROM Flowchart
Screened, excluded, and included number of randomised controlled
trials.
Found at doi:10.1371/journal.pmed.0040107.sd001 (24 KB PPT).
Acknowledgments
We thank Dr. Kiambo Njagi from the Ministry of Health, Nairobi, Kenya,
and Prof. Pascal Magnussen from the Danish Bilharzia Laboratory,
Copenhagen, Denmark, for provision of a copy of Dr. Njagi’s Ph.D.
dissertation. PJE was supported by a Fellowship Programme grant from
the Cochrane Infectious Diseases Group through the Effective Health
Care Research Programme Consortium at the Liverpool School of
Tropical Medicine, supported by the Department for International
Development. FOtK was supported by a grant from WHO and the US
Centers for Disease Control and Prevention.
This is an edited version of a Cochrane review available on the
Cochrane Library 2006 disk issue 2[28]. Cochrane reviews are
updated as new evidence emerges. The Cochrane Library should be
consulted for the most recent version of the review.
Author contributions. PG conceived the idea for the study. CG and
PJE designed the study. PG coordinated the analysis. CG, PJE, and
FOtK analyzed the data. FOtK and CG wrote the first draft, and all
authors contributed to subsequent versions of the paper.
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Insecticide-Treated Nets in Pregnancy
Editors’ Summary
Background. Malaria is one of the world’s most important killer diseases.
It is responsible for around a million deaths every year, most of them in
Africa and most of them in children. Pregnant women and their unborn
babies are also at high risk. Women who have malaria become extremely
weak because of anemia, they are more likely to miscarry, and their
babies have low birth weights. (Birth weights under 2.5 kilograms are
considered to be low; low-birth-weight babies face higher risks of
sickness and death than other babies.) It has been estimated that, every
year, malaria during pregnancy is responsible for the deaths of about
100,000 to 200,000 babies within their first year of life.
The parasite that causes malaria is carried by certain species of
mosquito. In the areas where these mosquitoes are found, taking steps
to reduce the chance of being bitten can reduce one’s chances of
getting infected with malaria. In Africa, these mosquitoes bite mainly in
the hours of darkness, so sleeping under a mosquito net helps. During
the last 20 years it has been established that mosquito nets impregnated
with an insecticide provide much better protection than ordinary nets.
Research has shown that children who sleep under these insecticide-
treated nets (ITNs) are much less likely to get malaria than other children
living in the same area. The correct use of ITNs is now being heavily
promoted in many national and international programs.
Why Was This Study Done? It seems logical that pregnant women
should be encouraged to sleep under ITNs, and this is recommended by
the World Health Organization and other authorities. However, we
cannot be sure that there are benefits, as there is a lack of clear evidence
to show whether women who sleep under ITNs actually suffer less from
malaria and anemia, and what the implications are for their babies.
What Did the Researchers Do and Find? They did no new work in the
field or in the laboratory. Instead, they conducted what is known as a
systematic review. Working to a set of criteria carefully formulated in
advanc e, they searched the medical literature for well-conducted
‘‘ randomized controlled trials’’ (RCTs) involving the use of ITNs by
pregnant women. RCTs are studies where one group of people receives
the ‘‘ treatment’’ under investigation and another group does not. It is
decided at random who goes into which group. The authors found five
trials in Africa, four of which fulfilled the entry criteria for their analysis. In
three of the four studies conducted in Africa, whole villages had been
‘‘ randomized’’ to determine which pregnant women received ITNs. In
another African trial, individual women had been randomized. In total,
over 6,000 women were involved in the African trials. One trial had been
done outside Africa, in Thailand, where just over 400 individual women
had been randomized.
In the research done in Africa, it had been found that women who
slept under ITNs had lower numbers of parasites in their blood.
Miscarriages were much reduced—by a third in those women who were
in their first few pregnancies. The overall proportion of babies who were
low birth weight went down by nearly a quarter. In the research done in
Thailand, the women using ITNs were less anemic and the miscarriage
rate was again lower, although there was no change in the low-birth-
weight figures.
What Do These Findings Mean? The evidence from the three trials
done in Africa strongly suggests that it is a good idea for pregnant
women to sleep under ITNs. With evidence available from only one trial
conducted outside Africa, it is hard to be sure at this stage whether ITNs
have the same beneficial effects for pregnant women in other parts of
the tropics. More research is needed there.
Additional Information. The following organizations all have useful
information about malaria on their Web sites, and we have provided links
to the appropriate pages below. Please access these Web sites via the
online version of this summary at http://dx.doi.org/10.1371/journal.
pmed.0040107.
US Centers for Disease Control and Prevention has information
specifically about malaria during pregnancy
Roll Back Malaria has information specifically about malaria during
pregnancy
Wikipedia—a free online encyclopedia that anyone can edit
The World Health Organization (WHO)
The United Nations Children’s Fund (UNICEF)
MedlinePlus brings together authoritative information from the US
National Library of Medicine, National Institutes of Health, and other
government agencies and health-related organizations
The Wellcome Trust
PLoS Medicine | www.plosmedicine.org March 2007 | Volume 4 | Issue 3 | e1070515
Insecticide-Treated Nets in Pregnancy
    • "The impact of interventions offered through ANC (screening for high-risk pregnancy, micronutrient supplementation , intermittent presumptive treatment (IPT) and long-lasting insecticide treated bed nets (LLIN), management of chronic hypertension, screening and treatment of syphilis) on the reduction of PM has not been proven for some and remains to be qualified for others [32][33][34][35][36][37][38][39][40][41][42][43][44]. On the other hand, screening for syphilis, IPT and LLIN, screening and treatment of diabetes over the course of pregnancy, prenatal corticoids as well as screening and induction of labor in cases of intrauterine growth retardation (IUGR) are, of all these interventions, the ones for which there is some proof in terms of impact on reduction of PM [45][46][47][48][49][50][51][52]. As to screening and management of diabetes mellitus, some prospective studies have shown that adequate glycemic control and follow-up during pregnancy are a reasonable means to reduce stillbirth and numerous other complications like congenital anomalies and macrosomy [51][52][53] . "
    [Show abstract] [Hide abstract] ABSTRACT: Background The Democratic Republic of Congo (DRC) has a high rate of perinatal mortality (PMR), and health measures that could reduce this high rate of mortality are not accessible to all women. Where they are in place, their quality is not optimal. This study was initiated to assess the relationship between these suboptimal maternal, newborn and child health (MNCH) services and perinatal mortality (PM) in Lubumbashi, DRC’s second-largest city. Methods We conducted a prospective cohort study, comparing women who had no, low, moderate, or high numbers of antenatal care (ANC) visits; three different levels of delivery care; and who did or did not attend postnatal care (PNC). Women were followed for 50 days after delivery, with PM as the primary endpoint. Results Uptake of recommended prenatal interventions was between 11-43 % among ANC attenders, regardless of the frequency of their visits. PM was 26 per 1000. ANC attendance was associated with PM. Newborns of mothers who had the lowest attendance had a mortality two times higher than newborns of women who had not attended ANC (low visits: adjusted odds ratio (aOR) = 2.2; 95 % confidence interval (CI) = 1.4-3.8). However, moderate (aOR = 1.4; 95 % CI =0.7–2.2) and high (aOR = 1.3; 95 % CI 0.7–2.2) attendance were not statistically significantly associated with PM. PNC attendance was not significantly associated with lower PM (relative risk 0.4, 95 % CI 0.1–2.6). Emergency obstetric and newborn care (EmONC) was significantly associated with a reduction in mortality (aOR = 0.2; 95 % CI = 0.2–0.8), with an 84.4 % reduction among newborns at risk, and an overall reduction in mortality of 10 % for all births. Conclusion Perinatal mortality was high among the infants of women in the cohort under study (26 per 1000 live births). Availability of MNCH, specifically EmONC, was associated with lower perinatal mortality, and if this association is causal, might avert 84.4 % of perinatal deaths among newborns at high-risk.
    Full-text · Article · Dec 2016
    • "Several studies on ITN efficacy or effectiveness conducted have shown continued ability of ITNs protection against malaria transmission [9][10][11]. Moreover, studies on pregnancy outcome showed that use of bed nets could reduce miscarriages and stillbirths by 33 % and by 23 % in placental parasitaemia [12]. Overall, the use of ITNs have been effective [1, 7, 13] . "
    [Show abstract] [Hide abstract] ABSTRACT: Background: Although malaria decline has been observed in most sub-Saharan African countries, the disease still represents a significant public health burden in Tanzania. There are contradictions on the effect of ownership of at least one mosquito net at household on malaria mortality. This study presents a Bayesian modelling framework for the analysis of the effect of ownership of at least one mosquito net at household on malaria mortality with environmental factors as confounder variables. Methods: The analysis used longitudinal data collected in Rufiji and Ifakara Health Demographic Surveillance System (HDSS) sites for the period of 1999-2011 and 2002-2012, respectively. Bayesian framework modelling approach using integrated nested laplace approximation (INLA) package in R software was used. The space time models were established to assess the effect of ownership of mosquito net on malaria mortality in 58 villages in the study area. Results: The results show that an increase of 10 % in ownership of mosquito nets at village level had an average of 5.2 % decrease inall age malaria deaths (IRR = 0.948, 95 % CI = 0.917, 0.977) in Rufiji HDSS and 12.1 % decrease in all age malaria deaths (IRR = 0.879, 95 % CI = 0.806, 0.959) in Ifakara HDSS. In children under 5 years, results show an average of 5.4 % decrease of malaria deaths (IRR = 0.946, 95 % CI = 0.909, 0.982) in Rufiji HDSS and 10 % decrease of malaria deaths (IRR = 0.899, 95 % CI = 0.816, 0.995) in Ifakara HDSS. Model comparison show that model with spatial and temporal random effects was the best fitting model compared to other models without spatial and temporal, and with spatial-temporal interaction effects. Conclusion: This modelling framework is appropriate and provides useful approaches to understanding the effect of mosquito nets for targeting malaria control intervention. Furthermore, ownership of mosquito nets at household showed a significant impact on malaria mortality.
    Full-text · Article · Dec 2016
    • "Use of protection against mosquito bites may result in prevention of these diseases in addition to reducing mosquito annoyance and itching. For malaria control, insecticide-treated nets (ITNs) and indoor residual spraying are methods with proven efficacy, commonly used in elimination efforts [6][7][8][9] . In India, China and other countries , there is an extensive internal market for additional mosquito repellents providing personal protection; these include coils, vaporizers, mats and creams (Table 1). "
    [Show abstract] [Hide abstract] ABSTRACT: Background: Repellents such as coils, vaporizers, mats and creams can be used to reduce the risk of malaria and other infectious diseases. Although evidence for their effectiveness is limited, they are advertised as providing an additional approach to mosquito control in combination with other strategies, e.g. insecticide-treated nets. We examined the use of repellents in India in an urban setting in Chennai (mainly Plasmodium vivax malaria), a peri-urban setting in Nadiad (both P. vivax and P. falciparum malaria), and a more rural setting in Raurkela (mainly P. falciparum malaria).
    Full-text · Article · Jul 2016
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