Women’s Access and Provider Practices for the Case ......Women’s Access and Provider Practices...

Women’s Access and Provider Practices for the CaseManagement of Malaria during Pregnancy: A SystematicReview and Meta-AnalysisJenny Hill1*, Lauren D’Mello-Guyett1, Jenna Hoyt1, Anna M. van Eijk1, Feiko O. ter Kuile1, Jayne Webster2

1 Department of Clinical Sciences, Liverpool School of Tropical Medicine, Liverpool, United Kingdom, 2 Disease Control Department, London School of Hygiene & Tropical

Medicine, London, United Kingdom

Abstract

Background: WHO recommends prompt diagnosis and quinine plus clindamycin for treatment of uncomplicated malaria inthe first trimester and artemisinin-based combination therapies in subsequent trimesters. We undertook a systematic reviewof women’s access to and healthcare provider adherence to WHO case management policy for malaria in pregnant women.

Methods and Findings: We searched the Malaria in Pregnancy Library, the Global Health Database, and the InternationalNetwork for the Rational Use of Drugs Bibliography from 1 January 2006 to 3 April 2014, without language restriction. Datawere appraised for quality and content. Frequencies of women’s and healthcare providers’ practices were explored usingnarrative synthesis and random effect meta-analysis. Barriers to women’s access and providers’ adherence to policy wereexplored by content analysis using NVivo. Determinants of women’s access and providers’ case management practices wereextracted and compared across studies. We did not perform a meta-ethnography. Thirty-seven studies were included,conducted in Africa (30), Asia (4), Yemen (1), and Brazil (2). One- to three-quarters of women reported malaria episodesduring pregnancy, of whom treatment was sought by .85%. Barriers to access among women included poor knowledge ofdrug safety, prohibitive costs, and self-treatment practices, used by 5%–40% of women. Determinants of women’streatment-seeking behaviour were education and previous experience of miscarriage and antenatal care. Healthcareprovider reliance on clinical diagnosis and poor adherence to treatment policy, especially in first versus other trimesters(28%, 95% CI 14%–47%, versus 72%, 95% CI 39%–91%, p = 0.02), was consistently reported. Prescribing practices weredriven by concerns over side effects and drug safety, patient preference, drug availability, and cost. Determinants ofprovider practices were access to training and facility type (public versus private). Findings were limited by the availability,quality, scope, and methodological inconsistencies of the included studies.

Conclusions: A systematic assessment of the extent of substandard case management practices of malaria in pregnancy isrequired, as well as quality improvement interventions that reach all providers administering antimalarial drugs in thecommunity. Pregnant women need access to information on which anti-malarial drugs are safe to use at different stages ofpregnancy.

Please see later in the article for the Editors’ Summary.

Citation: Hill J, D’Mello-Guyett L, Hoyt J, van Eijk AM, ter Kuile FO, et al. (2014) Women’s Access and Provider Practices for the Case Management of Malariaduring Pregnancy: A Systematic Review and Meta-Analysis. PLoS Med 11(8): e1001688. doi:10.1371/journal.pmed.1001688

Academic Editor: Clara Menéndez, Hospital Clinic Barcelona, Spain

Received January 16, 2014; Accepted June 25, 2014; Published August 5, 2014

Copyright: � 2014 Hill et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricteduse, distribution, and reproduction in any medium, provided the original author and source are credited.

Data Availability: The authors confirm that all data underlying the findings are fully available without restriction. All relevant data are within the paper and itsSupporting Information files, and the published studies are available on the the Malaria in Pregnancy (MiP) Library (http://library.mip-consortium.org), the GlobalHealth Database (http://www.ebscohost.com/corporate-research/global-health), and the International Network for Rational Use of Drugs (INRUD) Bibliography(http://www.inrud.org/Bibliographies/INRUD-Bibliography.cfm).

Funding: This work was supported by a Master Service Agreement (contract # 20762) from the Bill & Melinda Gates Foundation to the Liverpool School ofTropical Medicine. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Competing Interests: The authors have declared that no competing interests exist.

Abbreviations: ACT, artemisinin-based combination therapy; AL, artemether-lumefantrine; ANC, antenatal care; AQ, amodiaquine; AS, artesunate; CAR, CentralAfrican Republic; CHW, community health worker; CQ, chloroquine; IDP, internally displaced person; IPTp, intermittent preventive treatment in pregnancy; RDT,rapid diagnostic test; SP, sulphadoxine-pyrimethamine; TBA, traditional birth attendant.

* Email: [email protected]

PLOS Medicine | www.plosmedicine.org 1 August 2014 | Volume 11 | Issue 8 | e1001688

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Introduction

Malaria in pregnancy is an important public health problem for

both maternal and neonatal health programmes. The manifesta-

tion of maternal infection with malaria depends on transmission

intensity, and prompt diagnosis and treatment of malaria illness in

pregnancy is important in all malaria endemic regions. Since

2006, WHO recommends quinine plus clindamycin for the

treatment of uncomplicated malaria in the first trimester, and

artesunate (AS) plus clindamycin for treatment failures. Artemi-

sinin-based combination therapies (ACTs) known to be effective in

the country/region, or AS plus clindamycin, are the recom-

mended combinations for case management of uncomplicated

malaria in the second and third trimesters [1,2]. Use of the

artemisinin class of compounds, alone or in combination therapies,

is not recommended in the first trimester of pregnancy because of

insufficient safety data in early pregnancy in humans [3], unless

this is the only treatment immediately available [1].

Many countries in high transmission settings have made ACTs

available free of charge to pregnant women in efforts to achieve

universal coverage [4]. Despite increasing availability of ACTs and

new diagnostic tools, such as rapid diagnostic tests (RDTs), very

little is known about women’s access to these interventions and

about the diagnosis and treatment practices of healthcare

providers. National malaria indicator surveys focus on access to

case management among children, the other important risk group

for malaria. Similarly, research on uptake of new diagnostics and

ACTs has to date focussed on children and non-pregnant adult

populations, whereas research on uptake of interventions in

pregnancy has predominantly focussed on progress and challenges

to the delivery and uptake of preventive interventions, namely,

intermittent preventive treatment in pregnancy (IPTp) and

insecticide-treated nets [5]. Information on access to and delivery

of effective case management of malaria in pregnancy has not yet

received the attention it deserves.

We undertook a systematic review of the factors affecting

pregnant women’s access to and health provider adherence to the

2006 WHO policy [2] on the treatment of malaria in pregnancy

globally. Among pregnant women we reviewed treatment-seeking

practices for malaria illness—the range of providers visited, the

antimalarials used, and the factors affecting their choice of

healthcare provider and medicines. We explored adherence to

policy among the range of healthcare providers administering

antimalarials to pregnant women, the type and quality of

diagnostic and case management services offered at the point of

care (including consideration of gestational age), and the health

system or other factors that affect quality of care.

Methods

Search StrategyStudies investigating treatment-seeking practices for malaria

among pregnant women and healthcare provider case manage-

ment practices for malaria in pregnancy were identified by

searching the Malaria in Pregnancy Library [6], the Global Health

Database [7], and the International Network for the Rational Use

of Drugs (INRUD) Bibliography [8] from 1 January 2006 to 3

April 2014. The Malaria in Pregnancy Library (http://library.

mip-consortium.org) is a comprehensive bibliographic database

created by the Malaria in Pregnancy Consortium that is updated

every 4 mo using a standardised protocol to search over 40

sources, including PubMed, Web of Knowledge, and Google

Scholar. Searches were run separately for ‘‘pregnant women’’ and

‘‘health providers’’ (see Table S1 for search terms), without

language restrictions, and both peer-reviewed and grey literature

were retrieved.

Study SelectionTitles and abstracts were reviewed independently for inclusion

by two reviewers (J. Hill and L. D9M-G/J. Hoyt). Studies wereincluded if they met the following criteria: (1) study contained data

on treatment seeking among women and/or case management

practices for malaria in pregnancy, (2) study population included

pregnant women and/or healthcare providers, (3) study reported

original research data, and (4) study was conducted following the

introduction of ACTs for the treatment of uncomplicated malaria

in pregnancy in the study country. No restrictions were placed on

study design (i.e., quantitative, qualitative, and mixed methods

studies), or quality of reporting. Studies limited to knowledge of

malaria in pregnancy amongst pregnant women, i.e., without

information on practices, were excluded. The Kappa (K) statistic

was used as a measure of the inter-rater agreement on study

eligibility between reviewers. Discrepancies between reviewers

were resolved through discussions with a third reviewer (J. W.)

until consensus was reached.

Studies meeting the inclusion criteria were assessed and grouped

according to content. Among pregnant women primary outcomes

included (1) treatment-seeking practices for malaria, (2) barriers to

accessing malaria treatment, and (3) determinants of treatment

seeking for malaria. Among healthcare providers primary

outcomes were (1) case management practices for malaria in

pregnancy, (2) factors affecting malaria case management practic-

es, and (3) determinants of knowledge, diagnosis, and treatment of

malaria.

Data ExtractionTwo authors extracted data and appraised the quality and

content of included studies. Data for pregnant women or

healthcare providers were extracted and analysed separately for

description and frequency of practices, barriers/facilitators, and

determinants (Figure 1). Two authors (J. Hill and L. D9M-G/A.M. v. E/J. Hoyt) extracted quantitative data on the type and

frequency of practices from quantitative and mixed methods

studies. For pregnant women these quantitative data included the

frequency of malaria episodes, sources of treatment, and the

resultant treatment achieved, and for healthcare providers the

quantitative data included the type and frequency of diagnostic

and treatment practices in relation to national drug policy at the

time of publication. J. Hill and L. D9M-G/J. Hoyt extractedqualitative and quantitative data on the barriers and facilitators to

treatment seeking among pregnant women and case management

practices among healthcare providers from qualitative and mixed

methods studies. J. Hill and L. D9M-G/J. Hoyt extractedquantitative data on the determinants of treatment seeking and

case management practices among pregnant women and health-

care providers, respectively, from quantitative and mixed methods

studies. For healthcare providers, determinants of knowledge and

practice, and of diagnosis and treatment, were extracted

separately. Two authors (J. Hill and L. D9M-G/J. Hoyt) assessedthe quality of reporting of individual studies using a checklist of

criteria developed a priori based on criteria and methods described

in the literature, described previously [5].

Data Synthesis and AnalysisNarrative synthesis was used to summarise, compare, and

contrast the type, range, and frequency of practices from each

study evaluating treatment seeking among pregnant women and

case management practices among healthcare providers. To make

Access to Case Management of Malaria in Pregnancy


http://library.mip-consortium.orghttp://library.mip-consortium.org

a comparison between national policy and healthcare provider

practices by country and region, we used the national or global

malaria policy cited in the included studies.

Barriers and facilitators were explored using content analysis

with a previously defined thematic framework for pregnant

women and healthcare providers [5]. NVivo version 9.2 (QSR

International) was used to generate an index of codes, which

identified each of the recurring barriers amongst pregnant women

and healthcare providers. The themes emerged as all the data

were analysed, working cyclically through the studies. Data from

the women’s perspective were categorised into individual, social/

cultural/household, environmental, and health system levels. Data

from providers were synthesised into a matrix that combined

operational levels of individual, organisational, health system, and

non-health system levels, together with the six health systems levels

of the WHO Health Systems Framework, which include

governance/leadership, service delivery, health workforce/human

resources, health information systems, finance, and medical

products/technologies [9–11].

We appraised the quality of reporting of each study using a

checklist of criteria based on methods described in a previous

review [5], as described and reported in Tables S2–S4.

Statistical AnalysisWe pooled the frequency data for source of treatment among

pregnant women and adherence to treatment policy among

healthcare providers across different types of providers using

random effect meta-analysis in Stata version 12 (StataCorp) and

Comprehensive Meta-Analysis (Biostat; http://www.meta-

analysis.com/), which was also used for sub-group analysis. We

used forest plots to visualise the extent of heterogeneity between

studies. For studies that reported source of treatment for more

than one episode of fever, we included the response to the first

episode [12]. For source of treatment among pregnant women, we

conducted sub-group analysis within each category for the

following: whether the question involved practice (i.e., women

with fever) or attitude (i.e., a hypothetical question, ‘‘if they had

fever…’’); health facility– or population-based enrolment; urban

or rural populations; and country of study (Nigeria, the country

contributing the majority of studies, versus other countries). For

adherence to treatment policy, we conducted sub-group analysis

for the following: trimester treated, the effect of staff cadre

(medical doctor versus others), and method of data collection (self-

administered questionnaire, interview, or record review). I2 wasused to quantify heterogeneity [13].

Results

Of 2,047 records retrieved from the database searches, 37

studies met the inclusion criteria (Figure 2)—13 studies in

pregnant women, 18 studies in healthcare providers, and six

studies in both pregnant women and healthcare providers; only

one study evaluated interventions. There was close agreement

between the reviewers on the review of full text articles (K = 0.84).

The majority of studies were conducted in Africa (30), with only

four studies conducted in Asia (two in India [14,15] and two in

Figure 1. Analysis strategy.doi:10.1371/journal.pmed.1001688.g001



http://www.meta-analysis.com/http://www.meta-analysis.com/

Cambodia [16,17]), one in Yemen [18], and two in Brazil [19,20].

Of the studies conducted in Africa, 17 were in west and central

Africa and 12 in east and southern Africa, and one study had sites

in east, west and southern Africa [21]. All but three studies were

cross-sectional surveys at the population or facility level. The

remaining studies included two longitudinal qualitative studies

[21,22] and a randomised controlled trial [23]. The study

characteristics are provided in Tables 1–3.

Quality of about half (14/27) of the quantitative studies was

assessed to be moderate-high (scored 6–8/10), with ten low-

moderate-quality studies (4–5/10) and three high-quality studies

(9–10/10) (Table S2). The quality criterion least often met among

these studies was the use of multivariate analysis. The four

qualitative studies were assessed as moderate-high quality (4–7/8),

with only one of the studies reporting saturation of themes (Table

S3). All six mixed methods studies were assessed as high quality (9–

10/11), though only one study reported use of multivariate

analysis (Table S4). Data on frequencies of practices, barriers/

facilitators, and determinants of access among women were

extracted from 13, 15, and four studies, respectively, and of policy

adherence among healthcare providers, from 24, 22, and ten

studies, respectively (Table 4).

Pregnant Women PerspectivesThe 19 studies that contributed data on the treatment-seeking

practices of pregnant women were undertaken in ten countries

across Africa (seven studies in east Africa, eight in west Africa, one

in southern Africa, one in central Africa, and one with sites in east,

west, and southern Africa) and in one country in Asia (Tables 1

and 3).

Description and frequency of practices among pregnant

women. The proportion of women reporting at least one

episode of malaria during their current or recent pregnancy

ranged from 25% to 75% of respondents in three population-

based [24–26] and three facility-based [14,27,28] studies in Africa

and Asia, with between 30% and 46% of women reporting two or

more episodes in Africa [25,27,28] (Tables 5 and 6). Of one

population-based [25] and three facility-based [14,28,29] studies,

a high proportion (.85%) of women with a reported episode ofmalaria during pregnancy sought some form of treatment.

Pregnant women in three population-based [26,30,31] and

seven facility-based [12,14,22,27–29,32] studies in Africa reported

self-medication or treatment at a pharmacy/drug store at the onset

of fever (range 5%–40%), and attended a health facility only if

their fever did not respond to this treatment [12,30] (Tables 5 and

6). In southern Ghana, women seeking treatment at a pharmacy or

drug vendor without a clinic prescription reported that the

antimalarials were selected by either the shop attendant (21% and

26% in rural and urban areas, respectively) or themselves (8% and

10%, respectively) [30]. Use of local herbs was a first resort among

pregnant women in a population-based study in Nigeria [33].

Pregnant women in urban settings were likely to seek care from

Figure 2. PRISMA chart of studies included in the review.doi:10.1371/journal.pmed.1001688.g002



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aN

atio

nal

Ru

ral/

urb

an2

00

8P

op

ula

tio

nC

ross

-se

ctio

nal

Qu

anti

tati

veM

D1

02

!!

Oko

ro2

01

2[4

0]

We

stA

fric

aN

ige

ria

,1

dis

tric

tU

rban

20

09

Faci

lity

Cro

ss-

sect

ion

alQ

uan

tita

tive

MD

31

1!

!!

Om

o-A

gh

oja

20

08

[37

]W

est

Afr

ica

Nig

eri

aN

atio

nal

Ru

ral/

urb

an2

00

6Fa

cilit

yC

ross

-se

ctio

nal

Qu

anti

tati

veM

D8

4!

!!

!

On

wu

jekw

e2

01

2[3

9]

We

stA

fric

aN

ige

ria

,1

dis

tric

tU

rban

20

10

Faci

lity

Cro

ss-

sect

ion

alQ

uan

tita

tive

MD

/nu

rse

/ph

arm

52

!!

!!

PSI

20

07

[16

]A

sia

Cam

bo

dia

Nat

ion

alR

ura

l/u

rban

20

07

Faci

lity

Cro

ss-

sect

ion

alM

ixe

dM

D/M

A/p

har

m/

nu

rse

/mid

wif

e/D

V7

50

!!

Smit

hP

ain

tain

20

11

[47

]W

est

Afr

ica

Gh

ana

7d

istr

icts

Ru

ral

20

09

Faci

lity

Cro

ss-

sect

ion

alM

ixe

dM

idw

ife

/nu

rse

/CH

W1

34

!!

!

Stan

ge

lan

d2

01

1[4

5]

East

Afr

ica

Ug

and

a,

1d

istr

ict

Ru

ral

20

09

Po

pu

lati

on

Cro

ss-

sect

ion

alM

ixe

dT

BA

28

!!

Taw

fik

20

06

[17

]A

sia

Cam

bo

dia

2d

istr

icts

Urb

an2

00

4P

op

ula

tio

nC

ross

-se

ctio

nal

Mix

ed

Ph

arm

/DV

70

!!

!

Um

ar2

01

1[3

8]

We

stA

fric

aN

ige

ria

1st

ate

Urb

an—

Faci

lity

Cro

ss-

sect

ion

alQ

uan

tita

tive

FHW

25

!!

!!



antenatal care (ANC) or health facilities as a first resort, as

observed in three population-based studies in Nigeria (42%) [24],

Sudan (82%) [31], and internally displaced person (IDP) camps in

Uganda (86%) [26], and five facility-based studies (range 63%–

92%) in Ethiopia [32], Nigeria [27–29], and India [14].

Data on sources of treatment extracted from nine studies

showed high heterogeneity across studies (I2 ranging from 60% to99%) (Figure 3), and all but one study [12] were of moderate to

high quality. Site of enrolment (health facility– versus population-

based), country (Nigeria versus other countries), and type of

question (practice versus attitude) had no effect within each

category (Table S5). Compared to urban women, rural women

were more likely to make use of a traditional healer or herbs (2%,

95% CI 0%–7%, three studies, versus 21%, 95% CI 6%–52%,

four studies, respectively, p = 0.008), whereas urban women mademore use of health facilities (84%, 95% CI 71%–91%, two studies,

versus 38%, 95% CI 14%–70%, four studies, p = 0.006).Only six of the 14 studies among pregnant women with

treatment-seeking practice as a primary outcome included

quantitative data on use of ACTs, and of these, only four stratified

use by trimester. In a household survey in Uganda, among first

trimester episodes, quinine was used in only 6% of first trimester

cases, with .80% of episodes treated with drugs not recom-mended for use in the first trimester either because they are

contraindicated (sulphadoxine-pyrimethamine [SP] and arte-

mether-lumefantrine [AL]) or because of high-grade drug

resistance (chloroquine [CQ]) [25]. Only 30% of second and

third trimester cases adhered to national guidelines (AL or quinine)

[25]. Another study conducted in 2011 in Uganda reported

appropriate treatment in only 36% of febrile cases, defined as

parasite-positive pregnant women given AL (Coartem) and

parasite-negative women given no antimalarial drug [34]. Of

pregnant women interviewed at a public hospital in Tanzania,

31% had used AL for an episode of malaria in the index

pregnancy, 27% SP, 23% quinine, 16% sulphalene-pyrimeth-

amine, and 3% amodiaquine (AQ) [35]. The majority (82%) of

women said they were asked about gestational age before being

given AL by drug dispensers; however, only 17% of pregnant

women were aware that AL should not be taken in the first

trimester, and only 22% knew that quinine was recommended. In

a population-based study in Ghana, drug sellers said some women

requested artemisinin combinations for treatment in the first

trimester [30].

A household survey in southeast Nigeria found that 42% of

pregnant women who had a fever within the last month had visited

a health facility, of which 46% were treated with ACTs, 34% with

SP, and 4% with artemisinin monotherapy; however, trimester

was not specified [24]. In an earlier population-based study in

Nigeria, women reported a high preference for SP for case

management in the second and third trimesters of pregnancy,

whereas the national treatment policy in second and third

trimesters was to use AL; the study was, however, done only a

year after the new policy was introduced [33]. A more recent

facility-based study in a teaching hospital reported that quinine

was used in only 12% of first trimester episodes, with artemisinin-

containing compounds, SP, and CQ used in 35%, 39%, and 14%

of cases, respectively [28]. In a comparative study of treatment

practices of second and third trimester episodes in public and

private health facilities, quinine was used in 4% of episodes in both

types of facility, with artemisinin monotherapy constituting the

most frequently prescribed drug (36%–39%) [29].

Barriers to care seeking for malaria among pregnant

women. The factors affecting treatment seeking for malaria

most frequently cited in the content analysis related to the

Ta

ble

2.

Co

nt.

Stu

dy

De

scri

pti

on

Pri

ma

ryO

utc

om

es

Stu

dy

Re

gio

nC

ou

ntr

yS

cale

Urb

an

/Ru

ral

Stu

dy

Ye

ar

Ta

rge

tP

op

ula

tio

nS

tud

yD

esi

gn

Da

taT

yp

eS

am

ple

NK

no

wle

dg

ea

nd

Pra

ctic

es

Ba

rrie

rsto

Ca

seM

an

ag

em

en

t

De

term

ina

nts

of

Ca

seM

an

ag

em

en

t

Dia

gn

ost

ics

Tre

atm

en

t

Wyl

ie2

01

0[1

5]

Asi

aIn

dia

2st

ate

sR

ura

l/u

rban

20

06

–2

00

8Fa

cilit

yC

ross

-se

ctio

nal

Qu

anti

tati

veP

W+H

P{

28

0!

!!

1H

eal

thp

rovi

de

rp

ract

ice

sin

ferr

ed

fro

mm

ed

ical

file

/AN

Cca

rd.

{ He

alth

pro

vid

er

pra

ctic

es

ob

serv

ed

.C

HW

,co

mm

un

ity

he

alth

wo

rke

r;D

V,d

rug

ven

do

r/d

rug

sto

re;F

HW

,fe

mal

eh

eal

thw

ork

er;

HP

,he

alth

pro

vid

er;

MA

,me

dic

alas

sist

ant;

MD

,me

dic

ald

oct

or;

ph

arm

,ph

arm

acis

t(t

rain

ed

);P

SI,P

op

ula

tio

nSe

rvic

es

Inte

rnat

ion

alR

ese

arch

and

Me

tric

s;P

W,

exi

tin

terv

iew

sw

ith

pre

gn

ant

wo

me

n.

do

i:10

.13

71

/jo

urn

al.p

me

d.1

00

16

88

.t0

02



Ta

ble

3.

Ch

arac

teri

stic

so

fst

ud

ies

rep

ort

ing

ou

tco

me

sfo

rb

oth

pre

gn

ant

wo

me

nan

dh

eal

thp

rovi

de

rs(s

ixst

ud

ies)

.

Stu

dy

De

scri

pti

on

NP

rim

ary

Ou

tco

me

(PW

/HP

)*

Stu

dy

Re

gio

nC

ou

ntr

yS

cale

Urb

an

/R

ura

lS

tud

yY

ea

rT

arg

et

Po

pu

lati

on

Stu

dy

De

sig

nD

ata

Ty

pe

Sa

mp

leP

WH

P1

23

45

6

DT

Kam

uh

abw

a2

01

1[3

5]

East

Afr

ica

Tan

zan

ia,

1d

istr

ict

Urb

an2

00

9–

20

10

Faci

lity

Cro

ss-s

ect

ion

alQ

uan

tita

tive

PW

+DV

20

02

00

!!

!!

!

Kw

ansa

-Be

ntu

m2

01

1[3

0]

We

stA

fric

aG

han

a1

dis

tric

tR

ura

l/u

rban

20

10

Po

pu

lati

on

Cro

ss-s

ect

ion

alQ

uan

tita

tive

PW

+MD

/nu

rse

/p

har

m9

59

12

6!

!!

!

Man

irak

iza

20

11

[36

]C

en

tral

Afr

ica

CA

R,

1d

istr

ict

Urb

an2

00

9Fa

cilit

yC

ross

-se

ctio

nal

Qu

anti

tati

veP

W+H

P1

56

5!

!!

!

Mb

on

ye2

01

0[5

2]

East

Afr

ica

Ug

and

a1

dis

tric

tR

ura

l/u

rban

—P

op

ula

tio

nC

ross

-se

ctio

nal

Qu

anti

tati

veP

W+T

BA

/DV

/CH

W2

,78

55

1!

!

Ob

iech

e2

01

3[2

8]

We

stA

fric

aN

ige

ria

,1

dis

tric

tU

rban

20

11

Faci

lity

Cro

ss-s

ect

ion

alQ

uan

tita

tive

PP

W+H

P1

42

8!

!!

Pe

ll2

01

3[2

1]

East

,w

est

,so

uth

ern

Afr

ica

Ke

nya

,G

han

a,M

alaw

i4

dis

tric

tsR

ura

l/u

rban

20

09

–2

01

1P

op

ula

tio

nA

nth

rop

olo

gic

alQ

ual

itat

ive

PW

+HP

39

01

37

!!

*Pri

mar

yo

utc

om

es

for

bo

thp

reg

nan

tw

om

en

and

he

alth

pro

vid

ers

:(1

)tr

eat

me

nt-

see

kin

gp

ract

ice

s,(2

)b

arri

ers

totr

eat

me

nt

see

kin

g,

(3)

de

term

inan

tso

ftr

eat

me

nt

see

kin

g,

(4)

kno

wle

dg

ean

dp

ract

ice

sfo

rca

sem

anag

em

en

to

fm

alar

ia(d

iag

no

sis/

tre

atm

en

t),

(5)

bar

rie

rsto

case

man

age

me

nt,

and

(6)

de

term

inan

tso

fca

sem

anag

em

en

t.1H

eal

thp

rovi

de

rp

ract

ice

sin

ferr

ed

fro

mm

ed

ical

file

/AN

Cca

rd.

CH

W,

com

mu

nit

yh

eal

thw

ork

er;

D,

dia

gn

ost

ics;

DV

,d

rug

ven

do

r/d

rug

sto

re;

HP

,h

eal

thp

rovi

de

r;M

D,

me

dic

ald

oct

or;

ph

arm

,p

har

mac

ist

(tra

ine

d);

PP

W,

po

stp

artu

mw

om

en

;P

W,

pre

gn

ant

wo

me

n;

T,

tre

atm

en

t.d

oi:1

0.1

37

1/j

ou

rnal

.pm

ed

.10

01

68

8.t

00

3



following: women’s knowledge and perceptions of risk, perceptions

and experience of drug safety, cost, and perceptions and

experience of healthcare provider and health facility factors

(Table 7). Women in one facility-based study [14] perceived

malaria during pregnancy as not especially dangerous, and the first

response in two population-based [30,31] and four facility-based

[12,14,22,32] studies was to rely on self-medication or herbal

treatments, and to seek medical advice only if the illness did not

improve. Over 50% of women in a facility-based study reported

delaying .2 d after first noticing symptoms before seeking care

Table 4. Data extracted for frequencies, barriers, and determinants by survey type.

Study Pregnant Women{ Healthcare Providers?

Frequencies Barriers Determinants Frequencies Barriers Determinants

Facility-based studies

Bin Ghouth 2013 [18] ! ! !

Kiningu 2013 [41] ! ! !

Luz 2013 [19] ! !

Luz 2013 [20] ! !

Mbonye 2013 [34] !

Obieche 2013 [28] ! !

Onwujekwe 2013 [29] ! !

Harrison 2012 [43] ! ! !

Minyaliwa 2012 [51] ! !

Okoro 2012 [40] ! !

Onwujekwe 2012 [39] ! ! !

Kamuhabwa 2011 [35] ! ! ! ! ! !

Manirakiza 2011 [36] ! ! !

Smith Paintain 2011 [47] ! ! !

Umar 2011 [38] ! ! !

Karunamoorthi 2010 [32] ! !

Launiala 2010 [22] !

Maiga 2010 [12] ! !

Sabin 2010 [14] ! !

Smith Paintain 2010 [23] !

Wylie 2010 [15] ! ! !

Enato 2009 [27] ! !

Omo-Aghoja 2008 [37] ! ! !

PSI 2007 [16] ! !

Population-based studies

Pell 2013 [21] ! !

Enato 2012 [44] ! !

Mbachu 2012 [24] ! ! !

Henry 2012 [26] ! !

Kalilani-Phiri 2011 [42] ! !

Kwansa-Bentum 2011 [30] ! ! ! !

Okonta 2011 [46] ! !

Sangaré 2011 [25] ! ! !

Stangeland 2011 [45] ! !

Mbonye 2010 [52] ! !

Adam 2008 [31] ! !

Sam-Wobo 2008 [33] ! !

Tawfik 2006 [17] ! !

Summary total 13 15 4 24 22 10

{Pregnant women: for frequency data, see Tables 5 and 6; barrier data, Table 7; determinant data, Table 8.?Healthcare provider: for frequency data, see Tables 9 and 10; barrier data, Table 11; determinant data, Table 12.PSI, Population Services International Research and Metrics.doi:10.1371/journal.pmed.1001688.t004



Ta

ble

5.

Sym

pto

ms

and

nu

mb

er

of

ep

iso

de

so

fm

alar

iain

pre

gn

ancy

,an

dp

erc

en

tag

ew

ho

sou

gh

ttr

eat

me

nt

by

sou

rce

,re

po

rte

db

yp

reg

nan

tw

om

en

:po

pu

lati

on

-bas

ed

stu

die

s.

Re

gio

nC

ou

ntr

yS

tud

yS

cale

N

Re

po

rte

da

nE

pis

od

eo

fM

ala

ria

inP

reg

na

ncy

Nu

mb

er

of

Ep

iso

de

sR

ep

ort

ed

pe

rP

reg

na

ncy

Pe

rce

nta

ge

of

Wo

me

nW

ho

So

ug

ht

Tre

atm

en

tS

ou

rce

of

Tre

atm

en

t

HC

F/A

NC

Pri

va

teC

lin

icR

eta

ilS

ect

or/

Ph

arm

acy

Se

lf-

Me

dic

ate

Tra

dit

ion

al

We

sta

nd

Ce

ntr

al

Afr

ica

Gh

ana

Kw

ansa

-Be

ntu

m2

01

1[3

0]

1d

istr

ict

95

9N

RN

RN

R2

5.4

%2

8.8

%1

5.4

%{

Nig

eri

aM

bac

hu

20

12

[24

]1

dis

tric

t8

98

25

.3%

(fe

ver)

NR

NR

42

.3%

Nig

eri

aSa

m-W

ob

o2

00

8[3

3]

1d

istr

ict

1,4

00

NR

65

.0%

of

PW

had

3–

4e

pis

od

es

of

mal

aria

that

year

(no

tcu

rre

nt

pre

gn

ancy

)

NR

68

.0%

‘

Ea

sta

nd

So

uth

ern

Afr

ica

Sud

anA

dam

20

08

[31

]1

dis

tric

t1

68

NR

NR

NR

81

.5%

‘9

.5%

Ug

and

aH

en

ry2

01

2[2

6]

1d

istr

ict

76

94

9.0

%in

pas

t2

mo

NR

NR

86

.0%

c/1

0.0

%4

.0%

Ug

and

aSa

ng

aré

20

11

[25

],

1d

istr

ict

50

06

6.8

%3

7.0

%h

ad2

+e

pis

od

es

of

mal

aria

inp

reg

nan

cy9

4%

of

rep

ort

ed

ep

iso

de

s

1M

ult

iple

resp

on

sean

swe

rs.

{ He

rbs;

,1

%so

ug

ht

pra

yers

,b

ath

s,w

ate

r,an

d/o

rsl

ee

p.

‘Sp

eci

fie

das

he

rbs.

‘8

.9%

spe

cifi

cally

sou

gh

ta

mid

wif

e.

c/ID

Pca

mp

sett

ing

.H

CF,

he

alth

care

faci

lity;

NR

,n

ot

rep

ort

ed

by

stu

dy

auth

ors

;P

W,

pre

gn

ant

wo

me

n.

do

i:10

.13

71

/jo

urn

al.p

me

d.1

00

16

88

.t0

05



Ta

ble

6.

Sym

pto

ms

and

nu

mb

er

of

ep

iso

de

so

fm

alar

iain

pre

gn

ancy

,an

dp

erc

en

tag

ew

ho

sou

gh

ttr

eat

me

nt

by

sou

rce

,re

po

rte

db

yp

reg

nan

tw

om

en

:fa

cilit

y-b

ase

dst

ud

ies.

Re

gio

nC

ou

ntr

yS

tud

yS

cale

N

Pe

rce

nta

ge

of

Wo

me

nW

ho

Re

po

rte

da

nE

pis

od

eo

fM

ala

ria

inP

reg

na

ncy

Nu

mb

er

of

Ep

iso

de

sR

ep

ort

ed

pe

rP

reg

na

ncy

Pe

rce

nta

ge

of

Wo

me

nW

ho

So

ug

ht

Tre

atm

en

tS

ou

rce

of

Tre

atm

en

t

HC

F/A

NC

Re

tail

Se

cto

r/P

ha

rma

cyS

elf

-M

ed

ica

teT

rad

itio

na

l

We

sta

nd

Ce

ntr

al

Afr

ica

Mal

iM

aig

a2

01

0[1

2]

,1

dis

tric

t2

10

NR

NR

NR

31

.4%

40

.0%

27

.6%

Nig

eri

aO

bie

che

20

13

[28

],

1d

istr

ict

42

86

9.4

%3

0%

rep

ort

ed

.1

ep

iso

de

84

.6%

of

rep

ort

ed

ep

iso

de

s7

7.4

%1

0.7

%1

2.0

%

Nig

eri

aO

nw

uje

kwe

20

13

[29

],

1d

istr

ict

64

7N

RN

RW

om

en

atte

nd

ing

pu

blic

faci

litie

s,9

5.3

%8

9.1

%5

.7%

5.2

%

Wo

me

nat

ten

din

gp

riva

tefa

cilit

ies,

98

.6%

92

.0%

2.3

%6

.0%

Nig

eri

aEn

ato

20

09

[27

]1

stat

e6

30

64

.1%

1e

pis

od

e,

53

.7%

;2

,2

7.3

%;

3,

6.3

%;

and

4+,

12

.7%

NR

78

.0%

22

.0%

Ea

sta

nd

So

uth

ern

Afr

ica

Eth

iop

iaK

aru

nam

oo

rth

i2

01

0[3

2]

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[27]. The choice of treatment was influenced by women’s

perceptions of the safety of drugs used during pregnancy, as

reported by three population-based studies [30,31,33] and one

facility-based study [35]. Fear and/or prior experience of side

effects to drugs also influenced treatment choices and adherence,

as reported by one population-based [21] and three facility-based

[14,23,35] studies. In northern Ghana, pregnant women identified

contradictions between messages provided in health facilities and

their own experiences of malaria [21].

The high cost of treatment prevented pregnant women from

using the formal health sector in rural population-based surveys in

Ghana [21,30], Kenya [21], and Nigeria [24]. Poverty was said to

be why women resorted to herbal remedies in Kenya and Ghana,

to avoid costs of both transport and medical care [21]. Other

barriers cited were user fees at formal health services [33] or the

cost of treatment in urban areas in population-based surveys in

Ghana [30] and facility-based studies in the Central African

Republic (CAR) [36] and India [14]. Lack of adequate care at

Figure 3. Prevalence of source of malaria treatment during pregnancy assessed in 18 studies with quantitative data. hf, healthfacility–based survey; pb, population-based survey.doi:10.1371/journal.pmed.1001688.g003



Ta

ble

7.

Co

nte

nt

anal

ysis

of

fact

ors

that

affe

cttr

eat

me

nt

see

kin

gfo

rm

alar

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on

gp

reg

nan

tw

om

en

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nd

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cili

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rsto

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ee

kin

gfo

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reg

na

nt

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me

nL

ev

el

Ind

ivid

ua

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ltu

ral/

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use

ho

ldE

nv

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nm

en

tal

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al

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ed

dan

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pre

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12

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kno

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me

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or

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health facilities [23] was an additional deterrent to using the health

facilities. Women in one study reported that they did not

understand the instructions given by dispensers regarding (AL)

dosage and duration of use [35]. On the other hand, women who

were concerned for their pregnancy status, who were aware of the

treatment options [22,23,30] and considered the drugs safe and

effective [14,25,30,35], and who trusted the health facility staff

[21,23] were more likely to seek treatment at health facilities.

Women in Ghana and Kenya generally valued diagnostic tests for

malaria (and other diseases) and associated testing with more

effective treatment [21].

Determinants of care seeking for malaria among

pregnant women. The range of determinants of treatment

seeking among pregnant women explored across the included

studies included education, prior experience of miscarriage, and

ANC use. The key findings are highlighted in Table 8; insufficient

data and lack of consistency in the indicators used prevented us

from performing a meta-analysis of pooled data. A higher level of

education was associated with correct knowledge of AL use in

pregnancy in Tanzania [35]. Prior use of ANC services and

previous experience of miscarriage were associated with increased

treatment seeking for malaria in IDP camps in Uganda [26].

Healthcare Provider PerspectivesThe 24 studies that contributed data on the diagnosis and

treatment practices of healthcare providers were undertaken in ten

countries, involving a range of cadres, including medical doctors

and nurses, pharmacists, drug vendors, traditional birth attendants

(TBAs), and community health workers (CHWs) (Tables 2 and 3).

Description and frequency of diagnostic practices. Malaria

diagnosis in pregnancy by public healthcare providers in the studies

conducted in Africa was predominantly performed on the basis of

clinical symptoms, as reported by one population-based study in

Ghana [30] and five facility-based studies in CAR [36] and Nigeria

[37–40]. The exceptions to this were microscopy use by private

sector providers in Nigeria [39] and by a provincial hospital in

Kenya [41] (Table 9). One population-based study in Malawi [42]

and three facility-based studies in Nigeria [37,38,43] reported a

combination of clinical and parasitological diagnosis by microscopy.

Providers at the community level in three population-based studies,

including private providers in Cambodia [17] and TBAs in Africa

[44,45], relied exclusively on clinical symptoms unless women could

produce prescriptions issued from clinics. Globally, few studies

reported healthcare providers using RDTs. In Africa, reports of

RDT use have been relatively recent (2011 in Malawi [42] and 2012

in Nigeria [39]), compared to in Asia (2007 in Cambodia [16]), and

only a fraction of providers reported using RDTs (range 22%–34%)

[16,39,42]. In a population-based survey of medical doctors and

pharmacists in Malawi, availability of tests, patient symptoms, and

cost were the main factors affecting choice of diagnostic test [42]. In

an observational study of ANC visits in eastern India, blood tests

were typically obtained if a patient complained of fever, though

enquiries into presence of fever in patients were made in only a

minority of patients [15].

Description and frequency of treatment knowledge and

practices. In west and central Africa, 11 studies on health

providers were conducted in Nigeria (eight studies), Ghana (two),

and CAR (one), where the national antimalarial treatment

guidelines stipulate quinine for treatment of uncomplicated malaria

in the first trimester and an ACT in the second and third trimesters

[30,36,39] (Table 10). Only two of the eight studies in Nigeria

[28,37–40,43,44,46] reported a relatively high proportion of

providers adhering to treatment policy. Onwujekwe et al. found

that more doctors, pharmacists, and nurses providing ANC services

Table 8. Data on the determinants of treatment-seeking behaviours for malaria in pregnancy by pregnant women.

Determinant Study Country Scale N Details

Age Kamuhabwa 2011 [35] Tanzania ,1 district 200 Age is not associated with knowledge of AL use in pregnancy

Henry 2012 [26] Uganda 1 district 769 Age is not associated with increased treatment seeking

Education Kamuhabwa 2011 [35] Tanzania ,1 district 200 A higher level of education in women was associated with correctknowledge of AL use in pregnancy (p,0.001)

Henry 2012 [26] Uganda 1 district 769 Women’s level of education was not associated with increasedtreatment seeking

Marital status Henry 2012 [26] Uganda 1 district 769 Marital status was not associated to increased treatment seeking

Parity/gravidity Kamuhabwa 2011 [35] Tanzania ,1 district 200 Parity/gravidity was not associated with knowledge of AL use inpregnancy

Henry 2012 [26] Uganda 1 district 769 Gravidity was not associated with increased treatment seeking

Sangaré 2011 [25] Uganda 1 district 500 There was no difference between multiparous and primiparouswomen in their use of the recommended dosage of treatment

Gestational age Kamuhabwa 2011 [35] Tanzania 1 district 200 Age of gestation was not associated with knowledge of AL usagein pregnancy

Henry 2012 [26] Uganda 1 district 769 Age of gestation was not associated with increased treatmentseeking

Experience ofmiscarriage

Henry 2012 [26] Uganda 1 district 769 Prior experience of miscarriage was associated with increasedtreatment seeking (p = 0.049)

Prior use of ANC Henry 2012 [26] Uganda 1 district 769 Prior use of ANC services by women was associated with increasedtreatment seeking (p = 0.029)

SES Mbachu 2012 [24] Nigeria 1 district 898 SES of women was not associated with the utilisation of differentantimalarials by pregnant women

All effects measured using the Chi-squared test.SES, socio-economic status.doi:10.1371/journal.pmed.1001688.t008



Ta

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rov

ide

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of

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alt

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Date post:	27-Jan-2021
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