Introduction
Anaemia is a major factor in women's health, especially reproductive health in developing
countries. Severe anaemia during pregnancy is an important contributor to maternal
mortality [1], as well as to the low birth weight which is in turn an important risk
factor for infant mortality [2]–[3]. Even moderate anaemia makes women less able to
work and care for their children [4]. The causes of anaemia are multi-factorial, including
diet, infection and genetics, and for some of the commonest causes of anaemia there
is good evidence of the effectiveness of simple interventions: for example, iron supplementation
[5], long-lasting insecticide nets and intermittent preventive treatment for malaria
[6]–[7].
Hookworm infection has long been recognized among the major causes of anaemia in poor
communities [8], but understanding of the benefits of the management of hookworm infection
in pregnancy has lagged behind the other major causes of maternal anaemia. An epidemiological
study in 1995 highlighted the paradox presented to public health workers that an estimated
one-third of all pregnant women in developing countries were infected with hookworm
and yet, in the absence of safety data, the appropriate advice then current was to
avoid the use of anthelmintics in pregnancy [9]. Furthermore, the lack of an acceptable
intervention constrained the development of evidence-based understanding of the impact
of hookworm infection on maternal anaemia [10]. These issues were addressed directly
by de Silva and colleagues [11], who analysed the safety profile of some 20 years
of mebendazole use in antenatal clinics in Sri Lanka. In 2002, WHO published new guidance
indicating that pregnant women should be treated for hookworm infection, ideally after
the first trimester [12]. This immediately provided the opportunity for improved service
delivery, and also encouraged studies to assess the contribution of hookworm to anaemia
in pregnancy and the impact of treatment, some of which have been undertaken since
2002. These provide a rich new source of data to help inform public health decision
making, and in this paper we present a systematic review of hookworm as a risk factor
for anaemia among pregnant women. We also estimate the extent of the problem of hookworm
among pregnant women living in sub-Saharan Africa, where hookworm remains an intractable
reproductive health problem.
Methods
Data sources and search strategy
A systematic search of published articles was undertaken in July 2007 and repeated
again in October 2007. The online databases MEDLINE (1970–2007) and EMBASE (1980–2007)
were used to identify relevant studies, using the Medical Subject Headings (MSHs)
pregnancy or pregnant AND hookworm, Necator americanus, Ancylostoma duodenale, intestinal
parasites, geohelminths or soil-transmitted helminths AND an(a)emia, h(a)emoglobin
or h(a)ematocrit. All permutations of MSHs were entered and each search was conducted
twice to ensure accuracy. The search did not exclude non-English language papers.
The abstracts of returned articles were then reviewed, and if they did not explicitly
investigate the association between hookworm and anaemia, they were discarded. Potentially
useful articles were retrieved. We also reviewed reference lists of identified articles
and hand searched reviews. Where suitable papers did not provide information in a
relevant format, authors were emailed and requested to provide relevant summaries
of data. SB undertook the literature search and scanned the results for potentially
relevant studies, retrieved the full article, and contacted authors. SB and PJH independently
assessed every relevant paper, with no disagreements arising, and SB used a pre-formed
database to abstract information.
We followed the reporting checklist of the Meta-analysis of observational studies
in epidemiology (MOOSE) group [13]. The primary outcome analysis was haemoglobin concentration
(Hb), and our hypothesis was that haemoglobin concentration is associated with the
intensity of hookworm infection. Data without quantitative measures of Hb and hookworm
infection intensity were excluded. No distinction could be made between the two different
hookworm species, Necator americanus and Ancylostoma duodenale, because none of the
studies used specific methods to differentiate the species, and routine coprology
is unable to do this. Studies had to be based on at least 30 individuals. No scoring
of quality of studies was undertaken. However, a description of statistical methods
employed, including whether adjustment for potentially confounding variables, is provided.
For randomised controlled trials, information is provided on key components of study
design as recommended by the CONSORT statement [14].
Data analysis
Data were stratified according to the intensity of infection, based on thresholds
recommended by WHO: light (1–1,999 epg); moderate (2,000–3,999 epg); and heavy (4000+
epg). Estimates of Hb were assessed for each intensity category and differences between
categories were presented as a standardized mean difference (SMD) and 95% confidence
interval. These were calculated with a random-effects model according to the DerSimonian
and Laird method [15]. Heterogeneity was assessed by the I2 test with values greater
than 50% representing significant heterogeneity. When heterogeneity between studies
was found to be significant, pooled estimates were based on random-effect models and
the Hedges method of pooling. Results were displayed visually in forest plots. Bias
was investigated by construction of funnel plots and by the statistical tests developed
by Begg & Mazumdar [16] and Egger et al. [17]. Analysis was performed using the ‘metan’
and related functions in STATA version 10 (College Station, TX).
Estimating population at-risk of hookworm-related anaemia
We attempted to estimate the number of pregnant women infected with hookworm in hookworm-endemic
countries in sub-Saharan Africa. To estimate the number of pregnant women, we used
population data from the Gridded Population of the World (GPW) version 3.0 β [18].
GPW3.0β is a global human population distribution map derived from areal weighting
of census data from 364,111 administrative units to a 2.5′×2.5′ spatial resolution
grid. Country-specific medium variant population growth rates and proportions of the
female population aged 15–49 years available from the United Nations Population Division
– World Population Prospects [UNPD-WPP] database [19] were used to project this age
cohort of the population total to 2005 using ArcView (Environmental Systems Research
Institute Inc., CA, USA). The number of pregnant women was estimated separately for
each country from the crude birth rate (number of births over a given period divided
by the person-years lived by the population over that period); this will be an under-estimate
as it does not include women experiencing miscarriages and stillbirths, which are
not routinely reported. Hookworm prevalence was defined on the basis of an existing
model which uses satellite-derived climatic factors to predict the geographical distribution
and prevalence of hookworm among school-aged children [20]. In the absence of relevant
empirical data, we assume that infection prevalence is equivalent in school-aged populations
and pregnant women; this is probably an under-estimate since hookworm prevalence is
generally higher in adult populations [21]. We also assume that no large-scale hookworm
control has been undertaken. Extractions of population at risk by prevalence of hookworm
were then conducted in ArcView 3.2.
Results
Our literature searches identified 105 citations and from this list 30 potentially
relevant research studies were identified; the remaining citations were either research
studies among non-pregnant women, reviews or editorials. Of these 30 potentially relevant
studies, 19 were determined to be eligible, including 13 cross-sectional studies,
2 randomised controlled trials, 2 non-randomised treatment trials and 2 observational
studies.
Association between hookworm infection and haemoglobin
13 studies presented observational data on the relationship between hookworm infection
and haemoglobin concentration: eight from Africa, three from Asia and two from Latin
America. The characteristics of the cross-sectional studies included are presented
in Table 1. The data were stratified according to the intensity of infection. In four
of the studies, none of the woman included had an intensity of infection that exceeded
2,000 epg; in eight studies women had an infection intensity that exceeded 4,000 epg.
Comparing uninfected women and women lightly (1–1,999 epg) infected with hookworm,
the standardized mean difference (SMD) in Hb was −0.72 (95% CI: −1.26 to −0.18) (n = 13),
indicating that even women lightly infected with hookworm have lower Hb levels than
uninfected women. However, there was variation in the differences observed and examination
of forest plots suggested heterogeneity of effect, which was statistically significant
(I2 score of 72.9%). This was explained by inclusion of the study by Rodríguez-Morales
et al. [22] which collated data from nine states across Venezuela. Omitting this study
from the analysis, the SMD between women uninfected and lightly infected was −0.24
(95% CI: −0.36 to −0.13) (Figure 1). Omission of other studies made little or no difference
to the overall effect. There was slight evidence of bias using the Egger test (p = 0.008)
and the Begg test (p = 0.07): the relatively small study by Ayoya et al. [23] in Mali
showed evidence of effects that differed from the larger studies. Heavy hookworm infection
was also significantly associated with a lower Hb level compared to light infection:
the standardized mean difference in Hb was −0.57 (95% CI: −0.87 to −0.26) (n = 7)
(Figure 2). No evidence of bias was observed.
10.1371/journal.pntd.0000291.g001
Figure 1
Forest plot of the difference in haemoglobin (Hb) concentration among pregnant women
uninfected with hookworm and women harbouring a light (1–1,999 eggs/gram) hookworm
infection.
Standardised mean difference less than zero indicate lower Hb levels in lightly infected
women compared to uninfected women. The diamond represents the overall pooled estimates
of the effect of light hookworm infection on Hb.
10.1371/journal.pntd.0000291.g002
Figure 2
Forest plot of the difference in haemoglobin (Hb) concentration among pregnant women
women harbouring a light (1–1,999 eggs/gram) hookworm infection and women harbouring
a heavy (4,000+ eggs/gram) infection.
Standardised mean difference less than zero indicate lower Hb levels in heavily infected
women compared to lightly infected women. The diamond represents the overall pooled
estimates of the effect of heavy hookworm infection on Hb.
10.1371/journal.pntd.0000291.t001
Table 1
The impact of hookworm infection on haemoglobin concentration in pregnant women.
Setting
Participants and year of study
Prevalence of parasites (%)a
Prevalence of anaemia (threshold used)
Statistical methods and potential confounders adjusted fora
Study
Liberia
128 women attending antenatal clinic aged 14–43 y, 88% in 1st or 2nd trimester, 1985
Hw = 30.0
78% (<110 g/L)
Unadjusted t-test.
[50]
Kilifi, Kenya
251 women attending antenatal clinic aged 15–41 y, 88% in 1st–3rd trimester, 1993
Hw = 74.9Pf = 23.6
75.6% (<110 g/L)
Unadjusted Kruskal-Wallis test
[51]
Ashanti Region, Ghana
205 women attending antenatal clinic aged 15–49 y, who were healthy, in 3rd trimester
and resident in the area, 2003–2005
Hw = 8.1Pf = 35.1
57.1% (<100 g/L)
Unadjusted t-test.
[52]
Bamako, Mail
131 randomly selected women attending antenatal clinic aged 18–45 y, who were healthy,
in 1st–3rd trimester and resident in the area, 2002
Hw = 8Pf = 11
47% (<110 g/L)
Multivariate logistic regression: age, gestation, trimester, SES, abnormal vaginal
discharge, food constraints, Pf & Sh.
[23]
Ukerewe Island, Tanzania
972 women attending antenatal clinics aged 15–45 y, who were healthy and resident
in the area, 2004
Hw = 56.3Pf = 16.4Sm = 63.5
66.4% (<110 g/L)
Multivariate logistic regression: age, trimester, Pf & Sm.
[53]
Entebbe, Uganda
2507 women attending antenatal clinic aged 14–47 y, who were healthy and resident
in the area, 2003–2005
Hw = 44.5Pf = 10.9
39.7% (<112 g/L)
Multivariate logistic regression: age, SES & gravidity.
[54]
Masindi, Uganda
802 women attending first antenatal visit aged 14–42 y, who were healthy and resident
in the area,2003–4
Hw = 66.6Pf = 35.2
20.8% % (<100 g/L)
Multivariate logistic regression: age, gravidity, gestation, iron deficiency, Pf,
Sm, Al &Tt.
[55]
Pemba Island, Tanzania
857 women attending antenatal clinic aged 15–49 y, who were healthy, in 3rd trimester
and resident in the area, 2004
Hw = 32.9Pf = 7.4
Severe anaemia: 5.5% (<70 g/L)
Multivariate logistic regression: age, gestation, gravidity, SES, dietary intake,
iron deficiency, Hp & Pf.
[56]
Iquitos, Peru
1042 women attending antenatal clinics aged 18–42 y living in rural and peri-urban
areas, 2003–4
Hw = 47.2Tt = 82.3Al = 63.9
47.3% (<110 g/L)
Multivariate logistic regression: age, SES, education, gestation, Al & Tt.
[57]
Nine states, Venezuela
1038 women attending antenatal clinics in rural and peri-urban areas, 2003–4
Hw = 8.1
65.1% (<120 g/L)
Relative risks adjusted for Al, Tt & other protozoan infections.
[22]
Papua New Guinea
30 women attending antenatal clinic for first time, 1985
Hw = 60Pf/Pv = 7
44% (<100 g/L)
Unadjusted t-test.
[58]
Sarlahi district, Nepal
334 women included in a community randomised trial of micronutritient supplementation
aged 15–40 y, 1994–1997
Hw = 74.2Pv = 10.9
73% (<110 g/L)
Multivariate logistic regression: age, gestation, SES, Pv & serum retinol.
[48]
Yen Thanh district, Vietnam
371 women living in 6 purposively selected communities, 2003
Hw = 21.5Pf/Pv = 0
43.7% (<110 g/L)
Multivariate logistic regression: education, dietary intake, gestation & Al.
[59]
a
Hw = hookworm; Pf = Plasmodium falciparum; Pv = Plasmodium vivax; Sm = Schistosoma
mansoni; Sh = S. haematobium; Tt = Trichuris trichiura; Al = Ascaris lumbricoides;
Hp = Helicobacter pylori. SES = socio-economic status.
Effect of anthelmintic treatment
Our literature search identified two randomised controlled trials (RCTs) on the impact
of anthelmintic treatment in pregnancy, two non-randomised intervention trials, and
two observational studies (Table 2). All the studies showed a benefit of deworming
for maternal or child health, but since a variety of outcomes measures were employed
it is difficult to compare study findings quantitatively. Both RCTs had clear objectives,
provided sample sizes calculations and undertook analyses adjusted for potentially
confounding factors, but only the RCT in Peru [24) presented a flow of participants
through each stage and baseline characteristics of each group, and stated there was
adequate concealment of assignment of participants. Of the two RCTs, only the one
in Sierra Leone demonstrated a statistically significant benefit of treatment, with
the decline in Hb during pregnancy 6.6 g/L less in women treated with albendazole
compared to untreated women [25]. The study also showed an additive impact of deworming
and iron-folate supplementation, with 13.7 g/L less decline in Hb over the course
of pregnancy compared to controls. The RCT in Peru found no impact of treatment on
Hb or mean birthweight but showed a significant decrease in the prevalence of very
low birthweight with anthelmintic treatment [24]. In the Sierra Leone RCT, no adverse
pregnancy outcomes were found to be linked to albendazole. The RCT in Peru found no
significant difference between the mebendazole and placebo groups in the frequency
of miscarriages, malformations, stillbirths, early neonatal deaths and premature babies
[24],[26].
10.1371/journal.pntd.0000291.t002
Table 2
The impact of anthelmintic treatment (mebendazole (MBZ) or albendazole (ABZ)) on the
health of pregnant women in the developing world.
Study
Country
Prevalence of STHa
Baseline prevalence of anaemia b
Study design
Participants
Interventions
Results
RCTs
[25]
Sierra Leone
Hw = 65% Al = 20% Tt = 74%
56.0%
Randomised placebo-controlled factorial trial of ABZ and iron-folate supplementation
(n = 125). Assignment using random numbers
Women aged 15–38 y attending antenatal clinic in first trimester, Hb>g/L, gestational
age <14 weeks at baseline
400 mg ABZ 36 mg ferrous gluconate plus 5 mg folic acid daily
Between 1st and 3rd trimester, Hb of women receiving ABZ declined 6.6 g/L less than
control; the corresponding value for deworming and iron-folate supplementation was
13.7 g/L
[24]
Peru
Hw = 47% Al = 64% Tt = 82%
47.2%
Double-blind randomised placebo-controlled trial or MBZ plus iron versus placebo plus
iron (n = 1042). Concealed assignment using random numbers
Women aged 18–44 y attending 12 antenatal clinics in second trimester, Hb>g/L, gestational
age <18–26 weeks at baseline, and not received treatment for 6 months
500 mg MBZ 60 mg ferrous sulphate daily for 1 month
No difference in maternal anaemia or mean birthweight between groups; however, lower
prevalence of very low birthweight babies in MBZ group
Non-randomised intervention trials
[27]
Cote d'Ivoire
Hw = 50 Al = 78%
NAc
Non-randomised drug trial
Women aged 15–38 y attending antenatal clinic
500 mg Pyrantel pamoate daily for three days
Decrease in severe anaemia and 6-month infant mortality; increase in birthweight
[28]
Sri Lanka
Hw = 41.4
65.4%
Non-randomised intervention trial of iron supplementation and anthelmintics (n = 115)
Randomly selected pregnant plantation workers
Unspecified (probably MBZ) 60 mg ferrous sulphate and 0.25 mf folic acid daily for
1–2 months
Anthelmintic treatment in addition to iron supplementation improved Hb more than iron
supplementation alone
Observational studies
[29]
Nepal
Hw = 74% Al = 59% Tt = 5%
NA
Non-randomised community-based study investigating receipt of ABZ and health (No doses = 58;
One dose = 543; Two doses = 2726)
Pregnant women previously enrolled in a cluster-randomised trial followed up 6 months
post-delivery.
400 mg ABZ
Decrease in severe anaemia and 6-month infant mortality; increase in birthweight
[30]
India
NA
68.7%
Pre-post (18 months) community based evaluation (n = 828) of deworming and iron-folate
supplementation.
Randomly selected pregnant women from two areas (one intervention; one control).
100 mg MBZ twice daily for three days plus 60 mg ferrous sulphate from fourth month
of pregnancy
Improvement in Hb (6.4–8.4 g/L according to trimester)
Adapted and expanded from [60].
a
Hw = hookworm; Al = Ascaris lumbricoides; Tt = Trichuris trichiura;
b
Defined as Hb<110 g/L; c Not available.
The two non-randomised intervention trials presented data on the impact of anthelmintic
treatment on Hb. A study in Cote d'Ivoire included 32 pregnant women treated with
pyrantel pamoate and showed that the prevalence of hookworm decreased by 93% and Hb
increased by 6 g/L over the course of the pregnancy [27]. A study in Sri Lanka also
showed that treatment increased Hb in pregnant women, and found that providing both
mebendazole and iron supplementation had a greater impact on Hb than iron supplementation
alone [28]. The observational study in Nepal compared women who had received anthelmintic
treatment to those who did not, and found that treatment had significant beneficial
effects on severe anaemia, birthweight and infant mortality [29]. The other observational
study on pregnant women, in India, also found that co-administration of mebendazole
and iron supplementation resulted in improved Hb [30].
Burden of hookworm in pregnant women in sub-Saharan Africa (SSA)
Using GPW3.0β population estimates and country-specific age-sex structures, we estimate
that in 2005 there were 148 million women of reproductive age (15–49 years) in hookworm
endemic countries in SSA. Overlaying this surface with our model of hookworm prevalence
we estimate that 37.7 million women of reproductive age are infected with hookworm.
On the basis of number of live births occurring in SSA, we estimated that the number
of pregnant women in SSA in 2005 was 25.9 million of which approximately 6.9 million
were infected with hookworm.
Discussion
That human hookworm infection results in intestinal blood loss which, in turn, can
contribute to anaemia is well-established [8]. What has remained unclear and hindered
public health policy and planning is the extent to which hookworm is associated with
anaemia during pregnancy. The results of our systematic review quantify this relationship
and confirm that heavy intensities of hookworm infection are associated with lower
levels of haemoglobin than light infection intensities. This finding corroborates
previous studies among school-aged children that show a relationship between infection
intensity and haemoglobin [31]–[33].
Over forty years ago, Roche & Layrisse [31] in their seminal study on hookworm anaemia
identified four conditions necessary to show an association between hookworm infection
and Hb: a large sample size; quantitative measures of haemoglobin and hookworm infection;
sufficient variation in infection levels; and few other competing causes of anaemia.
These conditions are also relevant to interpreting the current results: in particular,
the absence of estimates of hookworm intensity resulted in the exclusion of studies,
some of which, reported no association between hookworm infection and the risk of
anaemia [34]–[36]; while others reported a significant association [37]–[38]. Anaemia
in developing countries has multiple causes, including micro-nutrient deficiencies,
infectious diseases and inherited disorders [39], and as such, the observed relationship
between Hb and hookworm infection may be confounded by other causes of anaemia. Furthermore,
residual confounding may exist among studies which did not adjust for socio-economic
status, which may lead to an overestimation of association. However, nine of the 13
studies undertook some form of analysis which adjusted for potential confounding variables,
including dietary intake, gestation age, and co-infections (Table 1), thereby adding
weight to the observed associations; only four studies adjusted for socio-economic
status.
The contribution of hookworm infection to maternal anaemia is such that all women
of child-bearing age could benefit from periodic treatment in hookworm endemic areas,
and that women harbouring the heaviest infections are likely to benefit most. Previously,
a systematic review of randomised controlled trials investigating the impact of anthelmintic
treatment on haemoglobin among school-aged children concluded that treatment against
intestinal nematode infections resulted in an increase in haemoglobin of 1.71 g/L
(95% confidence intervals 0.70–2.73) [40]. However, there were a number of important
omissions in the study, including the failure to distinguished between different helminth
species or account for intensity of infection, which may have under-estimated the
true treatment effect [41]. The treatment studies among pregnant women reported here
found that albendazole was effective in reducing the decline in haemoglobin that typically
occurs during pregnancy [25], but that the effect was less apparent with mebendazole
[24]. This may reflect the lower efficacy of mebendazole versus albendazole in treating
hookworm infection [42],[43]. However, there is a trade-off between efficacy and safety
since mebendazole is poorly absorbed from the gut whereas albendazole is turned into
a sulfoxide metabolite that gets widely distributed in the tissues. In addition to
drugs used, there are other potential reasons accounting for the difference in the
observed impact of anthelmintic treatment on haemoglobin. These include higher intensities
of hookworm among women in Peru than among the women in the Sierra Leone study. In
addition, different underlying aetiologies of anaemia may be relevant, such differences
in iron deficiency anaemia and malaria and schistosome transmission intensity [39].
Finally, although we did not quantitatively assess the quality of the studies, reporting
of the RCT in Sierra Leone was incomplete and it is possible that there were methodological
differences that were associated with observed treatment effects [14].
Despite the potential benefits of anthelmintic treatment during pregnancy, few countries
have included deworming in their routine antenatal care (ANC) programmes, with only
Madagascar, Nepal and Sri Lanka doing so routinely. It is suggested that a fear of
adverse birth outcomes as well as a lack of safety data, especially country-specific
data, represents a barrier for many ministries of health including anthelmintics into
their ANC programmes. The evidence from the RCTs included in this review found no
evidence of an increased risk of adverse events following treatement. This is consistent
with other observational studies which have investigated the safety of mebendazole
in pregnant women (for a recent review of studies, see [26]). We feel that the findings
of the present paper make clear that hookworm in pregnancy is prevalent and important,
and we strongly encourage that a substantial review of the safety evidence is undertaken,
perhaps by WHO and its partners.
The finding that co-administration of deworming and iron supplements has a greater
impact on haemoglobin than deworming alone supports the assertion that deworming is
unlikely to replenish iron stores in the short term, and needs to be combined with
iron supplementation, particularly among populations whose diets is low in bioavailable
iron [10]. In addition, a review of the impact of malaria-related anaemia among pregnant
women in sub-Saharan Africa suggested that over a quarter of cases of severe anaemia
were attributable to malaria [44], while other evidence shows that anaemia burden
can be reduced effectively by anti-malarial intermittent preventive treatment (IPT)
[7]. An effective package to improve maternal anaemia should therefore ideally include
IPT, iron supplementation and anthelmintic treatment. Interestingly, a recent case
control study of the causation of severe anaemia in young children in Malawi also
concludes that hookworm has tended to be overlooked as a causal factor [45]. The value
of combining deworming with micronutrient supplementation for children has previously
been emphasized [46].
We found only slight evidence of publication bias, and this is likely to be less important
than the numerous other factors that may introduce heterogeneity [17], such as transmission
of malaria and schistosomiasis, iron and nutritional intake, diagnostic accuracy in
quantifying Hb and hookworm intensity. Furthermore, hookworm species may be important
but in the reported studies, no distinction was made between N. americanus and A.
duodenale because of the practical difficulties of differential diagnosis. Pathological
studies indicate that A. duodenale causes greater blood loss than N. americanus [47],
with epidemiological studies among Zanzibari schoolchildren suggesting that A. duodenale
is associated with an increased risk of anaemia [48]. Thus, where hookworm is exclusively
A.duodenale, such as in Nepal [49], the observed effect on maternal anaemia might
be greater.
In 1995, Bundy and colleagues estimated that in low income countries, 44 million (35.5%)
out of 124 million pregnant women were infected with hookworm [9]. Here we estimate
that 6.9 million (26.7%) out of 25.9 million pregnant women in SSA are infected with
hookworm. Our current estimates are more precise since they are the first to explicitly
include the fine spatial variation in distribution of both infection and population.
They suggest that the earlier methodology may have overestimated the proportion of
pregnant women infected. On the other hand, the reliance on infection prevalence data
from surveys of schoolchildren, in the absence of data from adult women, means that
both estimation procedures are likely to result in under-estimates. Nonetheless, the
estimates suggest that between a quarter and a third of pregnant women in sub-Saharan
Africa are infected with hookworm and therefore at risk of preventable hookworm-related
anaemia.
In conclusion, this systematic review presents evidence that increasing hookworm infection
intensity is associated with lower haemoglobin levels in pregnant women in poor countries.
The chronic and recurring nature of hookworm infection throughout the reproductive
years means that it may have a chronic impact on the iron status of infected women,
potentially contributing to their morbidity and mortality and that of their children.
In many developing countries it is policy that pregnant women receive anthelmintic
treatment but in practice coverage rates are often unacceptably low. We suggest that
efforts are made to increase the coverage of anthelmintic treatment and iron supplementation,
with, where appropriate, intermittent preventive treatment for malaria.