Ma e nal Mala ia and Malnu i ion
(M3) ini ia i e, a pooled bi h coho o
13 p egnancy s udies in A ica and he
Wes e n Pacific
Holge W Unge ,
1,2
Jo dan E Ca es,
3
Julie Gu man,
4
Vale ie B iand,
5,6
Nadine Fie e ,
5,6
Innocen Valea,
7,8
Halidou Tin o,
7,8
Umbe o d’Alessand o,
9,10,11
Sa ah H Landis,
12
Se h Adu-A a wuah,
13
Ka h yn G Dewey,
14
Feiko Te Kuile,
15
S ephanie Dellicou ,
15
Pe e Ouma,
16
Lau ence Slu ske ,
4
Dianne J Te louw,
17
Simon Ka iuki,
16
John Ayisi,
16
Be na d Nahlen,
18
Meghna Desai,
4
Mwayi Madani sa,
19
Linda Kalilani-Phi i,
15,19
Pe Asho n,
20,21
Kenne h Male a,
19
I o Muelle ,
22
Danielle S anisic,
23
Ch is en ze Schmiegelow,
24
John Lusingu,
24,25
Daniel Wes eich,
3
Anna Ma ia an Eijk,
15
S e en Meshnick,
3
S ephen Roge son
2
To ci e: Unge HW, Ca es JE,
Gu man J, e al. Ma e nal
Mala ia and Malnu i ion
(M3) ini ia i e, a pooled bi h
coho o 13 p egnancy
s udies in A ica and he
Wes e n Paci ic. BMJ Open
2016;6:e012697.
doi:10.1136/bmjopen-2016-
012697
▸P epublica ion his o y o
his pape is a ailable online.
To iew hese iles please
isi he jou nal online
(h p://dx.doi.o g/10.1136/
bmjopen-2016-012697).
Recei ed 17 May 2016
Accep ed 8 No embe 2016
Fo numbe ed a ilia ions see
end o a icle.
Co espondence o
P o esso S ephen Roge son;
s [email p o ec ed]
ABSTRACT
Pu pose: The Ma e nal Mala ia and Malnu i ion (M3)
ini ia i e has pooled oge he 13 s udies wi h he hope
o imp o ing unde s anding o mala ia–nu i ion
in e ac ions du ing p egnancy and o os e
collabo a ion be ween nu i ionis s and mala iologis s.
Pa icipan s: Da a we e pooled on 14 635 single on,
li e bi h p egnancies om women who had
pa icipa ed in 1 o 13 p egnancy s udies. The 13
s udies co e 8 coun ies in A ica and Papua New
Guinea in he Wes e n Paci ic conduc ed om 1996 o
2015.
Findings o da e: Da a a e a ailable a he ime o
an ena al en olmen o women in o hei espec i e
pa en s udy and a deli e y. The da a se comp ises
essen ial da a such as mala ia in ec ion s a us,
an h opome ic assessmen s o ma e nal nu i ional
s a us, p esence o anaemia and bi h weigh , as well
as addi ional a iables such ges a ional age a deli e y
o a subse o women. Pa icipa ing s udies a e
desc ibed in de ail wi h ega d o se ing and p ima y
ou come measu es, and summa ised da a a e a ailable
om each con ibu ing coho .
Fu u e plans: This pooled bi h coho is he la ges
p egnancy da a se o da e o pe mi a mo e de ini e
e alua ion o he impac o plausible in e ac ions
be ween poo nu i ional s a us and mala ia in ec ion in
p egnan women on e al g ow h and ges a ional
leng h. Gi en he cu en compa a i e lack o la ge
p egnancy coho s in mala ia-endemic se ings,
compila ion o sui able p egnancy coho s is likely o
p o ide adequa e s a is ical powe o assess mala ia–
nu i ion in e ac ions, and could poin owa ds se ings
whe e such in e ac ions a e mos ele an . The M3
coho may hus help o iden i y p egnan women a
high isk o ad e se ou comes who may bene i om
ailo ed in ensi e an ena al ca e including nu i ional
supplemen s and al e na i e o in ensi ied mala ia
p e en ion egimens, and he se ings in which hese
in e en ions would be mos e ec i e.
INTRODUCTION
I is es ima ed ha each yea o e 125 million
p egnan women esiding in low-income and
middle-income coun ies (LMICs) a e a isk
o in ec ion wi h Plasmodium alcipa um and
P. i ax.
1
Mala ia con ibu es o he high
bu den o ma e nal mo bidi y and mo ali y
in hese se ings and may a ec placen al
de elopmen and e al g ow h.
2
Seques a ion o P. alcipa um pa asi es in he
placen a has been associa ed wi h e al
g ow h es ic ion (FGR) and low bi h
weigh (LBW, <2500 g), hus con ibu ing o
S eng hs and limi a ions o his s udy
▪This coho pools da a om 14 635 single on,
li e bi h p egnancies in women who pa icipa ed
in 1 o 13 p egnancy s udies in a eas wi h high
bu dens o mala ia and unde nu i ion.
▪The Ma e nal Mala ia and Malnu i ion (M3)
pooled da a se uses da a collec ed a i s an e-
na al a endance and a ime o deli e y.
▪The da a se comp ises essen ial in o ma ion on
mala ia in ec ion s a us, ma e nal an h opome ic
indica o s o unde nu i ion, p esence o ma e -
nal anaemia, neona al an h opome ics and ges-
a ional age a deli e y, among o he s.
▪The main limi a ion is he he e ogenei y in a ail-
abili y o ce ain a iables due o s udy design
and da a collec ion di e ences be ween s udies.
Unge HW, e al.BMJ Open 2016;6:e012697. doi:10.1136/bmjopen-2016-012697 1
Open Access Coho p o ile
in an mo ali y and possibly long- e m heal h p o-
blems.
34
P. i ax has also been associa ed wi h ad e se
p egnancy ou comes.
5
Mala ia du ing p egnancy may
cause ma e nal anaemia, which i sel can ha e dele e i-
ous e ec s on e al de elopmen .
2
Ma e nal unde nu i-
ion is also common among p egnan women in hese
se ings,
6–8
and unde nou ished women a e mo e likely
o ha e g ow h- es ic ed e uses and babies wi h
educed bi h weigh .
9
To da e, i emains unclea
whe he he suscep ibili y o, and he impac o , mala ial
in ec ion a e a ec ed by ma e nal nu i ional s a us. A
small numbe o s udies sugges ha mac onu ien
nu i ional s a us modifies he e ec s o mala ia in p eg-
nancy, specifically he impac o P. alcipa um pa asi -
aemia on e al g ow h and bi h weigh .
10–12
Al hough
la gely o e looked, his may no be su p ising gi en ha
bo h mac onu ien and mic onu ien nu i ional s a us
a ec immune unc ion mo e b oadly.
13 14
As such,
he e may be scope o design in e en ions ha p e en
ad e se p egnancy ou comes by p o ec ing women and
hei o sp ing om he dele e ious consequences o
mala ia and unde nu i ion. This aligns wi h he 2015
Global S a egy o Women’s, Child en’s and
Adolescen s’Heal h ecommenda ions o educe he
isk o LBW and ma e nal anaemia h ough he p e en-
ion and ea men o mala ia and h ough adequa e
nu i ion du ing p egnancy.
15 16
The Mala ia in P egnancy Conso ium (MiPc), which
ecei es unding om he Bill & Melinda Ga es
Founda ion, b ings oge he scien is s whose aim is o
educe he bu den and impac o mala ia in p egnancy
in LMICs.
17 18
A he 2014 MiPc mee ing in New
O leans, Louisiana, USA, Conso ium membe s iden i-
fied he need o s udy he ela ionship be ween mac o-
nu ien nu i ional s a us and mala ia in p egnancy,
gi en he high p e alence o unde nu i ion in
mala ia-endemic coun ies. The MiPc and o he mala ia
esea che s ha e conduc ed a numbe o mala ia in
p egnancy s udies (obse a ional s udies and
andomised con olled ials (RCTs) o mala ia p e en-
ion s a egies) and many had collec ed ma e nal
an h opome ics and da a on anaemia. Simila ly, some
ecen ials o nu i ional supplemen a ion du ing p eg-
nancy collec ed mala iome ic indices. D awing on hese
da a, he e is a unique oppo uni y o s udy he
in e ac ion be ween unde nu i ion and mala ia,
oge he wi h o he isk ac o s such as ma e nal
anaemia.
The Ma e nal Mala ia and Malnu i ion (M3) ini ia i e
has pooled da a om 13 s udies wi h he hope o
imp o ing he unde s anding o mala ia–nu i ion in e -
ac ions and o os e collabo a ion be ween nu i ionis s
and mala iologis s. Reduc ion o LBW and anaemia we e
wo o he six global nu i ion a ge s o 2025 ag eed
on a he 2012 Wo ld Heal h Assembly.
15
As o 2014, he
Global Nu i ion Repo ound ha he e was li le p o-
g ess owa ds his a ge .
19
Risk ac o s o , and in e en-
ions o p e en , LBW a e all oo commonly s udied in
isola ion and wi hou c oss-discipline collabo a ion.
Topics o in e es o M3 include an e alua ion o
whe he mac onu ien unde nu i ion modifies he
impac o mala ia in ec ion du ing p egnancy; he in es-
iga ion o po en ial in e en ions ha add ess bo h
mala ia isk and nu i ional s a us du ing p egnancy;
and he s udy o he ole o anaemia in ela ion o
ad e se p egnancy ou comes.
POOLED COHORT DESCRIPTION
S udy popula ions
The M3 ini ia i e comp ises 13 s udies (7 RCTs and 6
coho s udies) conduc ed among p egnan women in
mala ia-endemic coun ies om 1996 o 2015.
10 20–32
S udies we e selec ed based on he a ailabili y o a p e-
de e mined se o essen ial a iables o each woman,
adequa e e hical clea ance and willingness o
collabo a o s o sha e da a. Essen ial a iables included
he assessmen o mala iome ic indices (ligh mic os-
copy (LM), quan i a i e PCR (qPCR) and/o apid diag-
nos ic es s (RDTs)) a en olmen /fi s an ena al ca e
isi (ANC), assessmen o an h opome ic indica o s a
en olmen (mid-uppe a m ci cum e ence (MUAC)
and/o body mass index (BMI)), g a idi y, ype o
mala ia p e en ion used and ma e nal age. Essen ial
deli e y ou comes included bi h weigh and newbo n
sex. Wi h bi h weigh being he p ima y ocus, we
es ic ed inclusion o women who deli e ed li e single-
on in an s wi hou congeni al abno mali ies, as p e i-
ously ecommended.
33
We included 14 635 single on, li e bi h p egnancies
om women who had pa icipa ed in 1 o 13 p egnancy
s udies ( able 1) conduc ed in se en coun ies in A ica
and one in he Wes e n Pacific(figu e 1, able 1). O
he se en RCTs, ou assessed he e ec i eness o di e -
en pha macological mala ia p e en ion egimens,
27–30
one addi ionally e alua ed nu i ional supplemen a-
ion,
21
one was designed solely o assess he e ec i eness
o nu i ional supplemen a ion
22
and one measu ed he
impac o insec icide- ea ed bed ne s (ITNs) on bi h
weigh .
25
The six p ospec i e coho s udies we e all
designed o assess isk ac o s and consequences o
mala ia in ec ion and/o an imala ial ea men du ing
p egnancy in di e en loca ions and among di e en
s udy popula ions.
10 20 23 26 31 32
Fo 10 o he 13 s udies, p egnan women we e iden i-
fied and ec ui ed a one o hei sel -ini ia ed ANC,
usually he booking isi
10 20 22 27–32
bu some imes a a
subsequen isi .
26
The EMEP s udy en olled women
ea ly in p egnancy, bu a subse o hese same women
we e also en olled in a c oss-sec ional s udy a deli e y,
he in e mi en p e en i e ea men in p egnancy
(IPTp)-MON s udy.
23 24
The Asembo Bay ITN coho
(Kenya) iden ified p egnan women h ough mon hly
communi y census, and he FSP/MISAME (Bu kina
Faso) s udy ec ui ed h ough a communi y-based
ne wo k o home isi o s.
21 25
Th ee s udies excluded
2Unge HW, e al.BMJ Open 2016;6:e012697. doi:10.1136/bmjopen-2016-012697
Open Access
Table 1 Cha ac e is ics o he 13 indi idual s udies included in he M3 ini ia i e
Coun ies S udy name Design Pe iod Median GA (IQR)* Mala ia p e en ion†
Nu i ional
in e en ion N‡n§
Benin STOPPAM I
20
Coho 2008–2010 17 (14–20) IPT-SP None 1037 791
BF FSP/MISAME
21 34
RCT 2006–2008 16 (11–21) IPT-SP(2), IPT-SP(3) MMS, FFS 1296 1020
DRC ECHO
10
Coho 2005–2006 19 (17–21) IPT-SP None 182 164
Ghana iLiNS-DYAD
22
RCT 2009–2012 17 (15–20) IPT-SP LNS, MMN, IFA 1320 1068
Kenya EMEP and IPTp-MON
23 24
Coho ¶ 2011–2013 23 (16–30) IPTp-SP None 1453 473¶
Kenya ITN
25
RCT 1996–1999 24 (20–30) IPT-SP s a ed du ing s udy None 911 711
Kenya Kisumu coho
26
Coho 1996–2001 36 (34–37) IPT-SP s a ed du ing s udy None 3155 3388**
Kenya STOPMIP
27
RCT 2012–2015 23 (20–26) IPT-SP, IPT-DHA-PQ, IST-DHA-PQ None 1546 1203
Malawi ISTp
28
RCT 2011–2013 21 (19–23) IPT-SP, IST-DP None 1873 1602
Malawi LAIS
29
RCT 2003–2006 20 (18–23) IPT-SP(2), IPT-SP(4) IPT-SPAZ None 1320 1190
PNG IPTp s udy
30
RCT 2009–2013 22 (19–25) IPT-SPAZ; Single dose SP and CQ None 2793 1943
PNG Sek coho
31
Coho 2005–2007 25 (22–28) Single dose SP and weekly CQ None 470 293
Tanzania STOPPAM II
32
Coho 2008–2010 19 (15–21) IPT-SP None 995 789
*Median (IQR): ges a ional age a en olmen assessed by e al biome y, o symphysis-pubis undal heigh when ul asound una ailable.
†I RCT, desc ibes he in e en ion, i coho , desc ibes he na ional policy du ing he s udy pe iod.
‡N, en olled in pa en s udy.
§n, li e bi h p egnancies ha me inclusion c i e ia o M3.
¶The EMEP s udy was a p ospec i e coho s udy wi h some o e lapping en olmen wi h he c oss-sec ional s udy IPTp-MON. One hund ed and ele en p egnancies we e en olled in EMEP and
IPTp-MON; in o ma ion on mala ia in ec ion a deli e y was ob ained o he subse o women in IPTp-MON.
**Includes addi ional women om a subs udy no included in he pa en s udy which o he wise me inclusion c i e ia o he pooled da a.
BF, Bu kina Faso; CQ, chlo oquine; DHA-PQ, dihyd oa emisinin-pipe aquine; DRC, Democ a ic Republic o he Congo; FFS, o i ied ood supplemen a ion; IFA, i on and olic acid
supplemen a ion; IPTp, in e mi en p e en i e ea men in p egnancy; IST, in e mi en sc eening o mala ia in ec ion; ISTp, in e mi en sc eening o mala ia in ec ion in p egnancy; ITN,
insec icide- ea ed bed ne ; LNS, lipid-based nu ien supplemen a ion; M3, Ma e nal Malnu i ion and Mala ia; MMS, mul iple mic onu ien s supplemen a ion; PNG, Papua New Guinea; RCT,
andomised con olled ial; SP, sulphadoxine-py ime hamine; SPAZ, SP and azi h omycin; STOPPAM, S a egies To P e en P egnancy Associa ed Mala ia.
Unge HW, e al.BMJ Open 2016;6:e012697. doi:10.1136/bmjopen-2016-012697 3
Open Access
HIV-in ec ed p egnan women,
22 27 28
h ee s udies did
no assess HIV s a us
21 30 31
and he emaining se en
s udies included bo h HIV-in ec ed and HIV-nega i e
p egnan women.
10 20 23 25 26 29 32
The p edominan mala ia species obse ed in all
s udies was P. alcipa um. The wo s udies in Papua New
Guinea (PNG) also epo ed P. i ax in ec ions.
30 31
Some s udies de ec ed P. o ale and P. mala iae in ec ions
bu p e alence was e y low (<1%). S udies no di e en-
ia ing be ween species (n=4) we e conduc ed in a eas
whe e P. alcipa um is he p incipal mala ia species, and
P. i ax is hough o be la gely absen .
20–22 25
Ele en
s udies epo ed high and pe ennial mala ia ansmis-
sion, while wo s udies epo ed medium- o-high pe en-
nial mala ia ansmission.
22 30
Measu emen s
Women in all s udies had a leas wo s udy isi s, a en ol-
men and deli e y, bu he equency and iming o
ollow-up isi s du ing p egnancy a ied by s udy. Gi en
logis ical and compu a ional in ensi y equi ed in pooling
longi udinal measu es and subs an ial he e ogenei y in e-
quency and iming o measu emen s, only da a a en ol-
men and a deli e y we e pooled om e e y s udy. Tables 2
and 3show a ailable en olmen and deli e y measu emen s
o each included coho . Measu emen s included bo h
hose a iables deemed essen ial o he main analyses on
mala ia, anaemia and malnu i ion, and hose a iables
deemed op ional bu in o ma i e. A ew measu emen s,
specifically mala ia in ec ion diagnos ics, malnu i ion
an h opome ics and anaemia diagnos ics wa an u he
discussion.
Mala ia in ec ion a en olmen
A en olmen , mala ia in ec ion was diagnosed by exam-
ina ion o pe iphe al blood.
35
Pa asi aemia was assessed
using one o mo e o he h ee ollowing app oaches:
LM examina ion o a Giemsa-s ained blood smea , qPCR
and RDTs ( able 2). In all bu wo s udies, mala ia a
en olmen was ou inely diagnosed by LM. In he FSP/
MISAME s udy in Bu kina Faso, LM was only pe o med
i a woman p esen ed wi h symp oms consis en wi h
mala ia, ha is, e e o his o y o e e .
21
In he
iLiNS-DYAD Ghana s udy, mala ia was only diagnosed
using an RDT.
22
RDTs de ec ci cula ing a ge mala ia
an igens and a e inc easingly used in mala ia-endemic
a eas when mic oscopy is no eadily a ailable.
35 36
Howe e , pe sis ence o ci cula ing a ge an igens a e
pa asi e clea ance can lead o alse-posi i e es esul s.
35
Sensi i i y o qPCR is much highe han LM and RDTs,
bu he ole o submic oscopic in ec ions de ec ed by
qPCR alone in causing ad e se ou comes has no been
clea ly de e mined.
37 38
Mala ia in ec ion a deli e y
In addi ion o pe iphe al blood diagnos ics a deli e y,
some s udies also assessed placen al mala ia in ec ion a
deli e y ( able 3). Placen al mala ia was diagnosed by
LM o a placen al blood smea , qPCR and/o placen al
his ology.
39
Th ee c i e ia a e used o classi y placen al
mala ia by his ology: p esence o in ec ed e y h ocy es;
haemozoin in monocy es/mac ophages and haemozoin
in fib in deposi s.
40
Placen al his ology is conside ed he
diagnos ic e e ence s anda d o placen al in ec ion.
MUAC and BMI
Ma e nal mac onu ien nu i ional s a us was assessed
by measu emen o women’s MUAC and/o BMI a
en olmen . MUAC, he ci cum e ence o he uppe a m,
assessed a he mid-poin be ween he elbow and he ip
o he shoulde , is equen ly used as a b oad indica o
o ma e nal p o ein ese es, a s o es and mac onu i-
en nu i ional s a us.
41
MUAC was measu ed in 10 o
he 13 s udies, which included 61% o ou o al s udy
popula ion ( able 2). Weigh and heigh ( o de i e BMI)
we e addi ionally measu ed in nine o hese s udies as
well as in he h ee s udies whe e MUAC was una ailable
( able 2). While nei he measu emen is pe ec , MUAC
Figu e 1 Geog aphical loca ions whe e he 13 pa en s udies we e conduc ed: Benin, Bu kina Faso, Democ a ic Republic o he
Congo, Ghana, Kenya, Malawi, Papua New Guinea and Tanzania.
4Unge HW, e al.BMJ Open 2016;6:e012697. doi:10.1136/bmjopen-2016-012697
Open Access
Table 2 Key measu es a en olmen ac oss he 13 s udies included in he M3 ini ia i e
Va iable STOPPAM-Benin
FSP/
MISAME-BF ECHO-DRC iLiNS-DYAD-Ghana
EMEP and
IPTp-MON-Kenya ITN-Kenya
Kisumu-
Kenya STOPMIP-Kenya ISTp-Malawi LAIS-Malawi IPTp-PNG Sek-PNG STOPPAM-Tanzania
Essen ial a iables
Mala ia
LM X X* X X X X X X X X X X
PCR XX XX
RDT X†X‡X§ X§ X†
An h opome ics
MUAC X* X X X X* X¶ X X X X
Weigh X X X X X X X X X X X X X
Heigh X X X X X X X X X X X X
G a idi y X X X X X X X X X X X X X
Anaemia**
Haemoglobin X X X X X X X X X X X X
Haema oc i X
Op ional a iables
Ges a ional age
Ul asound X X X X X* X X X* X
Fundal heigh X X* X X X* X X X X X X X X
Age X X X X X X X X X X X X X
Smoking (Y/N) X X X XXXX
HIV X X X X X* X X X X X
Residence
( u al/u ban)
XXXXXXXXXXXX
Bed ne owne ship X X X X X X X X X*
A ailable in o ma ion indica ed wi h X, missing da a >10% indica ed by *, and sys ema ically missing da a indica ed wi h g ey highligh ing.
†The STOPPAM Benin and Tanzania s udies p ima ily used he Pa asc een RDT (Zephy Biomedical Sys ems, Goa, India), which de ec s Plasmodium alcipa um HRP-2 and pLDH.
‡The iLiNS-DYAD-Ghana s udy used he Clea iew Mala ia Combo RDT (B i ish Biocell In e na ional, Dundee, UK), which de ec s HRP-2 and plasmodium aldolase.
§Women andomised o he ISTp a ms o he STOPMIP-Kenya and ISTp-Malawi s udies we e es ed wi h a Fi s Response Mala ia Ag. (pLDH/HRP2) Combo RDT (P emie Medical Co po a ion,
India).
¶Ma e nal MUAC measu ed a deli e y.
**Nine s udies measu ed haemoglobin using a HemoCue haemoglobinome e (Hemocue, Angelholm, Sweden),
20–22 26–31
one s udy elied on haemoglobin measu es om a local labo a o y (unknown
make),
23
one s udy used Sysmex hema ological analyse (Kobe, Japan)
32
and one s udy collec ed capilla y blood ( inge s ick) specimens o de e mina ion o haema oc i o haemoglobin le els using
a s anda dised cha .
10
In he ITN-Kenya s udy, haemoglobin was measu ed using a HemoCue haemoglobinome e (Hemocue, Angelholm, Sweden) be o e 1997, and om 1997 onwa ds capilla y
blood ( inge s ick) specimens we e collec ed o de e mina ion o haema oc i le els, which we e di ided by a ac o o h ee and p esen ed as haemoglobin alues o consis ency wi h he 1996 da a.
BF, Bu kina Faso; DRC, Democ a ic Republic o he Congo; HRP-2, his idine p o ein-2; IPTp, in e mi en p e en i e ea men in p egnancy; ISTp, in e mi en sc eening o mala ia in ec ion in
p egnancy; ITN, insec icide- ea ed bed ne s; LM, ligh mic oscopy; M3, Ma e nal Malnu i ion and Mala ia; MUAC, mid-uppe a m ci cum e ence; N, no; pLDH, Plasmodium lac a e dehyd ogenase;
PNG, Papua New Guinea; RDT, apid diagnos ic es ; STOPPAM, S a egies To P e en P egnancy Associa ed Mala ia; Y, yes.
Unge HW, e al.BMJ Open 2016;6:e012697. doi:10.1136/bmjopen-2016-012697 5
Open Access

Table 3 Key measu es a deli e y ac oss he 13 s udies included in he M3 Ini ia i e
Va iable
STOPPAM
-Benin FSP/MISAME-BF ECHO-DRC
iLiNS-DYAD
-Ghana
EMEP and
IPTp-MON-Kenya ITN-Kenya Kisumu-Kenya
STOPMIP
-Kenya ISTp-Malawi LAIS-Malawi IPTp-PNG Sek-PNG
STOPPAM
-Tanzania
Essen ial a iables
Mala ia—pe iphe al
LM X* X* X X*,†X X X X X* X X X
PCR X* X X
Mala ia—placen al
LM X* X* X*,†X X X X X* X* X*
PCR X X X* X* X*
His ology X X X X* X*
IPTp doses ecei ed X X* X X X X* X X X
Bi h weigh X X X X X X X X X X X X X
In an sex X X X X X X X X X X X X X
Op ional a iables
Ges a ional age
By ul asound X X X X X* X X X* X
Neona al an h opome ics
Abdomen ci cum e ence X* X XX
Ches ci cum e ence X X
Head ci cum e ence X X X X X X X X X X X
C own heel leng h X X X X X X X X
Timing o an h opome ics X X X X X X X X X X X X
A ailable in o ma ion indica ed wi h X, missing da a >10% indica ed by *, and sys ema ically missing da a indica ed wi h g ey highligh ing.
†Fo he EMEP/IPTp-MON s udy, only women co-en olled in he IPTp-MON s udy (n=111) had mala ia diagnos ics a deli e y.
BF, Bu kina Faso; DRC, Democ a ic Republic o he Congo; IPTp, in e mi en p e en i e ea men in p egnancy; ISTp, in e mi en sc eening o mala ia in ec ion in p egnancy; ITN,
insec icide- ea ed bed ne s; LM, ligh mic oscopy; M3, Ma e nal Malnu i ion and Mala ia; PNG, Papua New Guinea; STOPPAM, S a egies To P e en P egnancy Associa ed Mala ia.
6Unge HW, e al.BMJ Open 2016;6:e012697. doi:10.1136/bmjopen-2016-012697
Open Access
and BMI a e easy and low-cos nu i ional assessmen s
ha can be unde aken in low- esou ce se ings, and a e
clinically ele an .
42
Anaemia a en olmen
Mos women had haemoglobin measu emen s pe -
o med a fi s ANC, and mos ecei ed ou ine i on/
ola e supplemen s, al hough in o ma ion on hei use
was no ou inely collec ed. The dosage o ola e supple-
men a ion (0.4–5 mg) a ied by s udy si e.
FINDINGS TO DATE
Findings om each indi idual s udy emphasise how
pooling hese da a has he po en ial o gene a e impo -
an in o ma ion on mala ia–nu i ion in e ac ions in
p egnancy.
The ECHO s udy in he Democ a ic Republic o he
Congo (DRC) was he fi s s udy o epo an in e ac ion
be ween mala ia and malnu i ion on he isk o FGR.
10
In his s udy, he isk o FGR was 2–8 imes highe
among women wi h e idence o malnu i ion. In his
s udy, he magni ude o he di e ence in e ec sizes
depended on he measu emen o malnu i ion (BMI
s MUAC s sho s a u e s weigh gain) and he meas-
u emen o mala ia (c oss-sec ional s cumula i e);
howe e , wi h all measu emen s o malnu i ion and
mala ia, he pa e n and di ec ionali y o he modifica-
ion was consis en . This s udy, oge he wi h a small
numbe o ollow-up s udies, p o ided he necessa y p e-
limina y da a o he M3 ini ia i e.
712
Two pa icipa ing s udies p o ided e idence ega ding
nu i ional in e en ions du ing p egnancy. The FSP/
MISAME in Bu kina Faso s udy concluded ha mul iple
mic onu ien - o ified ood supplemen a ion inc eased
mean bi h weigh , and ha his e ec was mos p o-
nounced among women who we e anaemic o unde -
nou ished ea ly in hei p egnancy.
34
The iLiNS-DYAD
ial in Ghana ound modes o e all inc eases in bi h
weigh wi h he p o ision o lipid-based nu ien supple-
men s compa ed wi h i on and olic acid supplemen a-
ion, bu showed ha he in e en ion may be mos
e ec i e when gi en o p imipa ous women.
22
While
nu i ional assessmen was no he p ima y aim o he
emaining s udies, he IPTp RCT in PNG and he
S a egies To P e en P egnancy Associa ed Mala ia
(STOPPAM) coho s udy in Benin epo ed associa ions
be ween low ma e nal an h opome ics and bi h
weigh .
20 43
O he s udies la gely ocused on mala ia p e en ion.
In he la e 90s, he Kisumu coho s udy ound ha
implemen a ion o wo doses o IPT-sulphadoxine-
py ime hamine (SP) hal ed he p e alence o placen al
mala ia in ec ion. In ano he s udy conduc ed concu -
en ly in Kenya (Asembo Bay s udy) use o ITNs was
associa ed wi h a ma ked educ ion in placen al mala ia
and LBW, bu (as expec ed) wi h no appa en impac
on nu i ional s a us.
25
The LAIS s udy, conduc ed in
Malawi om 2003 o 2006, ound ha adding azi h omy-
cin o wo cou ses o mon hly SP (SPAZ) was be e a
educing mala ia a deli e y, LBW and p e e m bi h
han mon hly SP o wo doses o SP.
29 44 45
SPAZ was
also supe io when compa ed wi h he s anda d mala ia
p e en ion egimen used in PNG (SP plus chlo o-
quine),
30
whe e placen al in ec ion is an impo an isk
ac o o LBW.
31
The EMEP coho s udy ound ha
use o a emisinin combina ion ea men s du ing he
fi s imes e was no associa ed wi h inc eased isk o
misca iage.
23
The IPTp-MON s udy ound ha wi h
inc easing esis ance, he e ficacy o IPTp-SP in clea ing
exis ing in ec ions o p e en ing new ones is comp o-
mised; howe e , whe e he sex uple mu an is a e, i
emains associa ed wi h imp o emen s in bi h weigh
and ma e nal haemoglobin.
24
The STOPPAM coho s udies conduc ed in Benin
and Tanzania p o ided obse a ional da a on he e ec s
and po en ial limi a ions o wo-dose IPTp-SP.
Specifically, he STOPPAM-Benin s udy ound ha a sub-
s an ial p opo ion o women acqui ed mala ia in ec-
ions la e in p egnancy, some imes a e he second
IPTp dose had been gi en.
20
The STOPPAM-Tanzania
s udy also ound ha mala ia in ec ions in he fi s o
second imes e we e associa ed wi h al e ed e al
g ow h ha migh no be de ec able un il he hi d i-
mes e .
32
T ial da a om he FSP/MISAME s udy u he
co obo a ed hese obse a ional s udies; he FSP/
MISAME s udy ound ha mala ia in ec ion du ing he
fi s imes e was associa ed wi h highe isk o LBW
and ha addi ional doses o IPTp migh be mo e e ec -
i e.
21 46
These s udies, along wi h o he s, ha e high-
ligh ed he impo ance o ea ly and equen mala ia
p e en ion o imp o e bi h ou comes, and IPT-SP is
now ou inely gi en mon hly un il deli e y.
47 48
The in e mi en sc eening o mala ia in ec ion
(ISTp) Malawi s udy assessed ano he mala ia p e en-
ion s a egy by compa ing IPTp-SP wi h ISTp a ANC
isi s using RDTs and ea ing in ec ed women wi h
dihyd oa emisinin-pipe aquine (DHA-PQ).
28
The
STOPMIP Kenya s udy also assessed ISTp wi h DHA-PQ,
compa ing i o IPTp wi h DHA-PQ as well as IPTp-SP.
Analyses om bo h s udies sugges ha ISTp-DHA-PQ is
no supe io o he exis ing s a egy o IPTp-SP, al hough
IPTp-DHA-PQ was mo e e ec i e han bo h ISTp-DP
and IPTp-SP.
27
FUTURE PLANS
We plan o assess whe he ma e nal mac onu ien nu i-
ional s a us, as assessed by MUAC, BMI and ma e nal
heigh , al e s he isk o educed bi h weigh ha is
associa ed wi h mala ia in ec ion du ing p egnancy.
Among women who unde wen a da ing ul asound scan
in ea ly p egnancy, analyses will be pe o med using
p e e m bi h and small- o -ges a ional age as end poin s
in addi ion o LBW. To in o m policy decisions, we
u he plan o use ad anced epidemiological me hods
Unge HW, e al.BMJ Open 2016;6:e012697. doi:10.1136/bmjopen-2016-012697 7
Open Access
o s ochas ically model he impac ha plausible a ge ed
an imala ial and nu i ional in e en ions du ing p eg-
nancy could ha e on he numbe o babies bo n LBW in
mala ia endemic a eas.
49–51
Addi ional u u e analyses
include, bu a e no limi ed o, he ollowing: he impac
o anaemia on LBW; he in e ac ion be ween anaemia
and mala ia wi h ega d o inc easing he isk o LBW;
he media ion o he e ec o mala ia h ough anaemia
on LBW; and he use ulness and ag eemen o MUAC
e sus BMI o p edic ad e se bi h ou comes. Sho
ma e nal s a u e, po en ially indica i e o s un ing and
educed adolescen ca ch-up g ow h (ch onic unde nu-
i ion), has also been associa ed wi h inc eased isks o
ad e se bi h ou comes and will be explo ed using his
pooled da a se .
52
Finally, we will assess a o emen ioned
ela ionships and e ec s among p egnan women wi h
HIV, a pa ien coho known o be a inc eased isk o
ad e se ou comes due o mala ia and malnu i ion.
53
STRENGTHS AND LIMITATIONS
This pooled bi h coho holds p omise as he la ges p eg-
nancy da a se o da e o add ess ques ions ega ding
mala ia and nu i ion ha a e o g ea impo ance o
ma e nal and in an heal h. P io esea ch on his opic
has been limi ed by insu ficien s a is ical powe o
examine he in e ac ion be ween mala ia and malnu i-
ion. The pooled M3 o e s he oppo uni y o o e come
his limi a ion by inc easing s a is ical powe and p ecision,
which is pa icula ly aluable o conduc ing subg oup ana-
lyses and in es iga ing in e ac ions. The subs an ial size o
he pooled da a se also acili a es he applica ion o igo -
ous me hodological app oaches o sys ema ically missing
da a, such as mul iple impu a ion by chained equa ions,
s anda disa ion, la en a iable me hods o ans o ma ion
o measu emen s o c ea e commensu a e measu es.
54 55
A ailabili y o indi idual-le el da a, a he han agg ega e
da a om each s udy, allows defini ions o exposu es and
ou comes o be ha monised. Indi idual-le el in o ma ion
on mala ia and malnu i ion u he enables implemen a-
ion o complex modelling o assess a ge ed an imala ial
and nu i ional in e en ions du ing p egnancy. The di e -
si y o s udy popula ions included in he M3 coho , o
example, wi h espec o loca ion, e hnici y, mala ia ans-
mission in ensi y, mala ia and nu i ion in e en ions,
heal h in as uc u e and HIV p e alence, could p o ide
impo an da a wi h ega d o gene alisabili y o ou find-
ings. Specifically, his le el o popula ion di e si y, coupled
wi h a ailabili y o da a on mul iple isk ac o s o LBW
and g ea e s a is ical powe o assess subg oup e ec s, may
allow he iden ifica ion o high- isk women who could
benefi mos om mo e in ensi e an ena al ca e, nu i-
ional supplemen s and al e na i e mala ia p e en ion egi-
mens, and o he se ings in which hese in e en ions
would be mos e ec i e.
The main limi a ions o he pooled da a se a e
ela ed o missing da a and he e ogenei y o he col-
lec ed da a. Fi s , in o ma ion ha was collec ed by all
s udies a ied, leading o sys ema ically missing da a on a
numbe o impo an a iables ( ables 2 and 3). The
limi ed a ailabili y o accu a ely measu ed ges a ional
age hinde s he abili y o conduc p e e m bi h and
small- o -ges a ional age analyses o he en i e da a se
( able 3), bu should allow o meaning ul subanalyses.
Second, exclusion o misca iages and s illbi hs may
cause selec ion bias (le unca ion) o some analyses,
gi en he possibili y o di e en ial a es o ea ly p eg-
nancy losses in ela ion o in ec ion and nu i ional
s a us.
56
We will assess his po en ial bias using da a on
misca iages and s illbi hs ex ac ed om a subse o
s udies.
21 23 27 28
Thi d, po en ial con ounde s such as
concomi an helmin h in ec ion and mic onu ien defi-
ciencies we e no measu ed in pa icipan s udies.
57 58
Fou h, while MUAC only modes ly changes h oughou
p egnancy, BMI ends o inc ease wi h ges a ional age:
ges a ional age-adjus ed BMI may be one app oach o
add ess his p oblem. Fi h, while we ha e in o ma ion
on HIV s a us o a majo i y o s udies, in o ma ion on
use o an i e o i al he apy (ART) was no ex ac ed,
and secula changes o e ime ega ding use and e fi-
cacy o ARTs could influence he compa abili y o esul s
ac oss s udies ha en olled HIV-in ec ed women. Finally,
since he in en ion was o concen a e on a eas o
mode a e- o-high P. alcipa um ansmission, we did no
include any s udies ep esen ing o he mala ia-a ec ed
egions such as Cen al/Sou h Ame ica and India.
COLLABORATION
The in es iga o s welcome collabo a ion o u u e p o-
jec s and in i e p oposals o addi ional analyses.
Fu he de ails can be ob ained by con ac ing SR (s o-
[email p o ec ed]) and HWU (hwunge @doc o s.
o g.uk).
Au ho a ilia ions
1
Depa men o Obs e ics and Gynaecology, Edinbu gh Royal In i ma y,
Edinbu gh, UK
2
Depa men o Medicine a he Dohe y Ins i u e, The Uni e si y o
Melbou ne, Pa k ille, Vic o ia, Aus alia
3
Depa men o Epidemiology, UNC-Chapel Hill, Chapel Hill, No h Ca olina,
USA
4
Mala ia B anch, Di ision o Pa asi ic Diseases and Mala ia, Cen e o Global
Heal h, Cen e s o Disease Con ol and P e en ion, A lan a, Geo gia, USA
5
Ins i u de Reche che pou le Dé eloppemen (IRD), Mè e e en an ace aux
in ec ions opicales (UMR216), Pa is, F ance
6
COMUE So bonne Pa is Ci é, Facul é de Pha macie, Uni e si é Pa is
Desca es, Pa is, F ance
7
Uni e de Reche che Clinique de Nano o, Ins i u de Reche che en Sciences
de la San é-DRO, Bobo-Dioulasso, Bu kina Faso
8
Depa emen de Reche che Clinique, Cen e Mu az, Bobo-Dioulasso, Bu kina
Faso
9
Medical Resea ch Council Uni , The Gambia
10
London School o Hygiene and T opical Medicine, UK
11
Ins i u e o T opical Medicine, An we p, Belgium
12
Wo ldwide Epidemiology, GlaxoSmi hKline, Uxb idge, UK
13
Depa men o Nu i ion and Food Science, Uni e si y o Ghana, Legon,
Acc a, Ghana
14
Depa men o Nu i ion, Uni e si y o Cali o nia, Da is, Cali o nia, USA
15
Depa men o Clinical Sciences, Li e pool School o T opical Medicine,
Li e pool, UK
8Unge HW, e al.BMJ Open 2016;6:e012697. doi:10.1136/bmjopen-2016-012697
Open Access
16
Kenya Medical Resea ch Ins i u e (KEMRI)/Cen e o Global Heal h
Resea ch, Kisumu, Kenya
17
Malawi-Li e pool-Wellcome T us Clinical Resea ch P og amme Li e pool
School o T opical Medicine, Li e pool, UK
18
P esiden ’s Mala ia Ini ia i e, Washing on DC, USA
19
School o Public Heal h and Family Medicine, College o Medicine,
Uni e si y o Malawi, Blan y e, Malawi
20
Tampe e Cen e o Child Heal h Resea ch, Tampe e, Finland
21
Depa men o Pedia ics, Uni e si y o Tampe e and Tampe e Uni e si y
Hospi al, Tampe e, Finland
22
Wal e and Eliza Hall Ins i u e, Pa k ille, Vic o ia, Aus alia
23
Ins i u e o Glycomics, G i i h Uni e si y, Gold Coas , Queensland, Aus alia
24
Facul y o Heal h Science, Depa men o Immunology and Mic obiology,
Cen e o Medical Pa asi ology, Uni e si y o Copenhagen, Copenhagen,
Denma k
25
Na ional Ins i u e o Medical Resea ch, Tanga Cen e, Tanga, Tanzania
Con ibu o s HWU and SR we e in ol ed in he concep ion o his s udy.
HWU, JG, VB, NF, IV, HT, Ud’A, SHL, SA-A, KGD, FTK, SD, PO, LS, DJT, SK,
JA, BN, MD, MM, LK-P, PA, KM, IM, DS, CS, JL, AM E, SM and SR we e
in ol ed in design and supe ision o da a collec ion o he pa en s udies.
JEC and HWU d a ed he wo k. All he au ho s c i ically e ised his a icle
and app o ed he inal manusc ip as submi ed.
Funding The STOPPAM p ojec , ‘S a egies To P e en P egnancy Associa ed
Mala ia’was suppo ed by he Eu opean Union’s Se en h F amewo k
P og amme (EU FP7); STOPPAM con ac numbe : 200889. STOPPAM I
(Benin) and STOPPAM II (Tanzania). The FSP/MISAME s udy (Bu kina Faso)
was unded by Nu i ion Thi d Wo ld, The Belgium Minis y o De elopmen ,
Flemish In e uni e si y Council, and F ench Minis y o De elopmen . The
ECHO s udy (Democ a ic Republic o he Congo) was unded by he
Depa men o Epidemiology, Uni e si y o No h Ca olina Chapel Hill, UNC
Gillings School o Global Public Heal h. The iLiNS-DYAD (Ghana) ial was
unded by a g an o he Uni e si y o Cali o nia, Da is om he Bill &
Melinda Ga es Founda ion. EMEP was pa ly suppo ed by he Mala ia in
P egnancy (MiP) Conso ium, which is unded h ough a g an om he Bill &
Melinda Ga es Founda ion o he Li e pool School o T opical Medicine, UK
(46099) and pa ly by he US Cen e s o Disease Con ol and P e en ion
(CDC), Di ision o Pa asi ic Diseases and Mala ia h ough a coope a i e
ag eemen wi h Kenya Medical Resea ch Ins i u e (KEMRI), Cen e o Global
Heal h Resea ch (CGHR), Kisumu, Kenya. The IPTp-MON s udy (Kenya) was
suppo ed by he CDC. The ITN p ojec (Kenya) was unded by he US Agency
o In e na ional De elopmen . The Special Heal h Suppo Fund om he
Royal Ne he lands Embassy (Nai obi, Kenya) p o ided addi ional suppo o
he s udy o he impac o ITN in p egnancy. The Kisumu s udy (Kenya) was
unded by US Agency o In e na ional De elopmen (g an numbe s
AOT0483-PH1-2171 and HRN-A-00-04-00010-02) and he Ne he lands
Founda ion o he Ad ancemen o T opical Resea ch. The STOPMIP s udy
(Kenya) was unded by he Mala ia in P egnancy (MiP) Conso ium, which is
unded h ough a g an om he Bill & Melinda Ga es Founda ion o he
Li e pool School o T opical Medicine, UK. The ISTp s udy (Malawi) was
unded by he Eu opean and De eloping Coun ies Clinical T ials Pa ne ship
(EDCTP). The LAIS s udy was suppo ed by g an s om he Academy o
Finland (g an numbe s 79787 and 207010), he Founda ion o Pedia ic
Resea ch in Finland, and he Medical Resea ch Fund o Tampe e Uni e si y
Hospi al. Azi h omycin and i s placebo we e p o ided ee o cha ge by P ize
(New Yo k, New Yo k, USA), which also p o ided unding o he PCR es ing
o he sexually ansmi ed in ec ions. The IPTp s udy (Papua New Guinea
(PNG)) was unded by he MiP Conso ium, h ough a g an om he Bill &
Melinda Ga es Founda ion (46099); he P eg ax Conso ium, h ough a g an
om he EU FP7-2007-HEALTH (PREGVAX 201588) and he Spanish
Go e nmen (EUROSALUD 2008 P og amme); and P ize , h ough an
in es iga o -ini ia ed esea ch g an (WS394663). The Sek s udy (PNG) was
suppo ed by AusAID (g an o PNG Ins i u e o Medical Resea ch (IMR)), he
Na ional Heal h and Medical Resea ch Council o Aus alia; Aus alian
Resea ch Council; Wellcome T us ; and Ve e ans A ai s Resea ch Se ice. The
Wal e and Eliza Hall Ins i u e is suppo ed by he NHMRC In as uc u e o
Resea ch Ins i u es Suppo Scheme and Vic o ian S a e Go e nmen
Ope a ional In as uc u e Suppo . JEC was unded by he Na ional Ins i u e
o Alle gy and In ec ious Diseases a he Na ional Ins i u es o Heal h
(P e-doc o al T aining in In ec ious Disease Epidemiology g an #5 T32
AI070114).
Compe ing in e es s None decla ed.
P o enance and pee e iew No commissioned; ex e nally pee e iewed.
Da a sha ing s a emen Resea che s can eques da a use by con ac ing SR
(s oge @unimelb.edu.au) and HWU ([email p o ec ed]k).
Open Access This is an Open Access a icle dis ibu ed in acco dance wi h
he e ms o he C ea i e Commons A ibu ion (CC BY 4.0) license, which
pe mi s o he s o dis ibu e, emix, adap and build upon his wo k, o
comme cial use, p o ided he o iginal wo k is p ope ly ci ed. See: h p://
c ea i ecommons.o g/licenses/by/4.0/
REFERENCES
1. Dellicou S, Ta em AJ, Gue a CA, e al. Quan i ying he numbe o
p egnancies a isk o Mala ia in 2007: a demog aphic s udy. PLoS
Med 2010;7:e1000221.
2. Umbe s AJ, Ai ken EH, Roge son SJ. Mala ia in p egnancy: small
babies, big p oblem. T ends Pa asi ol 2011;27:168–75.
3. Ba dají A, Sigauque B, Sanz S, e al. Impac o mala ia a he end o
p egnancy on in an mo ali y and mo bidi y. J In ec Dis
2011;203:691–9.
4. Ba ke DJ, Gluckman PD, God ey KM, e al. Fe al nu i ion and
ca dio ascula disease in adul li e. Lance 1993;341:938–41.
5. Nos en F, McG eady R, Simpson JA, e al. E ec s o Plasmodium
i ax mala ia in p egnancy. Lance Lond Engl 1999;354:546–9.
6. Bu ki TK. Mala ia and malnu i ion: Nige ’s win c ises. Lance
2013;382:587–8.
7. Unge HW, Ome-Kaius M, Ka l S, e al. Fac o s associa ed wi h
ul asound-aided de ec ion o subop imal e al g ow h in a
mala ia-endemic a ea in Papua New Guinea. BMC P egnancy
Childbi h 2015;15:83.
8. Hanson MA, Ba dsley A, De-Regil LM, e al. The In e na ional
Fede a ion o Gynecology and Obs e ics (FIGO) ecommenda ions
on adolescen , p econcep ion, and ma e nal nu i ion: “Think
Nu i ion Fi s ”.In J Gynaecol Obs e O O gan In Fed Gynaecol
Obs e 2015;131(Suppl 4):S213–53.
9. Black RE, Vic o a CG, Walke SP, e al. Ma e nal and child
unde nu i ion and o e weigh in low-income and middle-income
coun ies. Lance 2013;382:427–51.
10. Landis SH, Lokomba V, Anan h CV, e al. Impac o ma e nal mala ia
and unde -nu i ion on in au e ine g ow h es ic ion: a p ospec i e
ul asound s udy in Democ a ic Republic o Congo. Epidemiol In ec
2009;137:294–304.
11. G i in JB, Lokomba V, Landis SH, e al. Plasmodium alcipa um
pa asi aemia in he i s hal o p egnancy, u e ine and umbilical
a e y blood low, and oe al g ow h: a longi udinal Dopple
ul asound s udy. Mala J 2012;11:319.
12. McClu e EM, Meshnick SR, Lazebnik N, e al. A coho s udy o
Plasmodium alcipa um mala ia in p egnancy and associa ions wi h
u e oplacen al blood low and e al an h opome ics in Kenya. In
J Gynaecol Obs e 2014;126:78–82.
13. Ry e MJH, Kol e L, B iend A, e al. The immune sys em in child en
wi h malnu i ion—a sys ema ic e iew. PLoS ONE 2014;9:e105017.
14. Shanka AH. Nu i ional modula ion o mala ia mo bidi y and
mo ali y. J In ec Dis 2000;182(Suppl 1):S37–53.
15. B anca F, Piwoz E, Schul ink W, e al. Nu i ion and heal h in
women, child en, and adolescen gi ls. BMJ 2015;351:h4173.
16. WHO. WHO | Global S a egy o Women’s, Child en’s and
Adolescen s’Heal h, 2016–2030. (ci ed 2015 Sep 28). h p://www.
who.in /en i y/li e-cou se/pa ne s/global-s a egy/
global-s a egy-2016-2030/en/index.h ml
17. The Lance In ec ious Diseases. Pu ing mala ia in p egnancy i mly
on he agenda. Lance In ec Dis 2007;7:79.
18. Mala ia in p egnancy conso ium. h p://www.mip-conso ium.o g/
19. In e na ional Food Policy Resea ch Ins i u e. Global nu i ion epo
2014: ac ions and accoun abili y o accele a e he wo ld’s p og ess
on nu i ion. 2014. h p://cdm15738.con en dm.oclc.o g/u ils/ge ile/
collec ion/p15738coll2/id/128484/ ilename/128695.pd
20. Huynh B-T, Fie e N, Gbaguidi G, e al. In luence o he iming o
mala ia in ec ion du ing p egnancy on bi h weigh and on ma e nal
anemia in Benin. Am J T op Med Hyg 2011;85:214–20.
21. Valea I, Tin o H, D abo MK, e al. An analysis o iming and
equency o mala ia in ec ion du ing p egnancy in ela ion o he isk
o low bi h weigh , anaemia and pe ina al mo ali y in Bu kina Faso.
Mala J 2012;11:71.
Unge HW, e al.BMJ Open 2016;6:e012697. doi:10.1136/bmjopen-2016-012697 9
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