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Spatial patterns and determinants of malaria

infection during pregnancy in Zambia

Article in Transactions of the Royal Society of Tropical Medicine and Hygiene · July 2015
DOI: 10.1093/trstmh/trv049

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Transactions of the Royal Society of Tropical Medicine and Hygiene Advance Access published July 9, 2015

Trans R Soc Trop Med Hyg 2015

doi:10.1093/trstmh/trv049

ORIGINAL ARTICLE
Spatial patterns and determinants of malaria infection during
pregnancy in Zambia
Mulakwa Kamuliwoa, Karen E. Kirkb, Emmanuel Chandac, Maha A. Elbadryd,e, Jailos Lubindaf,
Thomas A. Weppelmannd,e, Victor M. Mukonkag, Wenyi Zhangh, Gabriel Mushingei, Mercy Mwanza-Ingwea
and Ubydul Haqued,j,*

a
Ministry of Health, National Malaria Control Centre, Lusaka, Zambia; bIndependent Consultant, Baltimore, MD, USA; cVector Control
Specialist/Consultant, 11 Granite Street, Plot 33421/917 Kamwa South, Lusaka, Zambia; dEmerging Pathogens Institute, University of
Florida, Gainesville, FL, USA; eDepartment of Environmental and Global Health, College of Public Health and Health Professions, University
of Florida, Gainesville, FL, USA; fMacha Research Trust, Macha, Zambia; gDepartment of Public Health, Copperbelt University, School of

Downloaded from http://trstmh.oxfordjournals.org/ at OUP site access on July 10, 2015

Medicine, Ndola, Zambia; hInstitute of Disease Control and Prevention, Center for Disease Control, Beijing, People’s Republic of China;
i
Zambian Ministry of Environment and Statistics, Lusaka, Zambia; jDepartment of Geography, University of Florida, Gainesville, FL, USA

*Corresponding author: E-mail: ubydul.kth@gmail.com

Received 19 January 2015; revised 26 April 2015; accepted 18 May 2015

Background: Malaria in pregnancy (MiP) is a major concern in Zambia. Here we aim to determine the burden and
risk factors of MiP.
Methods: Monthly reported district-level malaria cases among pregnant women (count data) from January 2009
to December 2014 were obtained from the Zambian District Health Information System. Negative binomial regres-
sion model was used to investigate the associations between vector control tools, coverage of health care facilities,
transportation networks and population density. Data on MiP treatment were obtained from the 2012 Zambian
Malaria Indicator Survey. Yearly clusters of MiP were investigated using spatial statistics in ArcGIS v 10.1.
Results: The results indicated that MiP decreased in Zambia between 2010 and 2013. MiP was observed throughout
the year, but showed a strong seasonal pattern. Persistent hotspots of MiP were reported in the southeast and
northeast regions of Zambia, with districts that had better access to rail road and presence of water bodies asso-
ciated with decreased prevalence of MiP. Better indoor residual spraying and long-lasting insecticide-treated nets
coverage was demonstrated to be protective against MiP.
Conclusions: Mapping the distribution of MiP to track the future requirements for scaling up essential disease-
prevention efforts in stable hotspots can help the Zambian National Malaria Control Center to further develop
strategies to reduce malaria prevalence in this vulnerable sub-population.

Keywords: Diagnosis, Malaria, IPTp, Pregnancy, Risk factors, Zambia

Background Long-lasting insecticide-treated nets (LLINs) were initially dis-

Malaria in pregnancy (MiP) is defined as having a positive diagnosis
of malaria during pregnancy and is associated with maternal
anemia, prematurity, intra-uterine growth retardation, and low
birth weight.1 Worldwide, MiP contributes significantly toward
maternal and neonatal mortality, accounting for 10 000 maternal
and 200 000 neonatal deaths annually.2 Pregnant women living in
endemic areas are at greater risk of acquiring malaria infection and
developing severe malaria.2 Approximately 25 million pregnancies
occur each year in malaria endemic areas of sub-Saharan Africa.3
In 2010, it was estimated that over 716 000 pregnant women in
Zambia were at risk of malaria.3
tributed among pregnant women in Zambia through antenatal
clinics, using a subsidized voucher system. LLINs were also pro-
vided free-of-charge at first attendance to antenatal care (ANC)
clinics.4 No data was collected on ownership of LLINs among
pregnant women in Zambia in the 2007 Malaria Indicator
Survey (MIS).6 However, data were obtained from other studies
conducted between 2007 and 2012 that found the number of
pregnant women in Zambia who slept under an LLIN increased
from 43% to 58%.5,6 In 2012, more pregnant women slept
under LLINs in Zambia5,6 compared to the previous years (2006,
2008 and 2010).7 In general, LLIN coverage was high in
Zambia8 compared to other sub-Saharan African countries.9

# The Author 2015. Published by Oxford University Press on behalf of Royal Society of Tropical Medicine and Hygiene. All rights reserved.
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1
M. Kamuliwo et al.
Malaria continues to be a large source of maternal mortality in
malaria endemic areas of Zambia.10,11 In 2007, the maternal
mortality rate for Zambia was estimated at 591 deaths per
100 000 live births.12 This number decreased to 315 per
100 000 live births in 2013.13 Though overall maternal mortality
rates had declined by 4.1% (from 475 to 315 per 100 000 live
births) between 2003 and 2013, malaria continued to be a
major cause of mortality among pregnant women in the coun-
try.9,10 However, data from the 2007 Demographic Health
Survey (DHS) and the 2008 MIS found that approximately 94%
of pregnant women received ANC during some point in their preg-
nancy.6 WHO recommends effective case management to reduce
MiP and maternal mortality rates in high transmission areas
by improving access to intermittent preventive treatment in preg-
nancy (IPTp) using sulfadoxine-pyrimethamine (SP).14,23 Zambia’s
IPTp treatment case management protocol recommends three
doses of SP.12 In 2008, 60% of pregnant women received two or
more doses of SP/Fansidar for malaria prevention6 and in 2012
this number increased to 70%.6
The National Malaria Control Center (NMCC) in Zambia has
focused on identifying strategies to achieve relatively high
coverage of malaria interventions including distribution of
LLINs, indoor residual spraying (IRS), and IPTp coverage.
Despite the high MiP burden in the country, there has been rela-
tively little research on MiP at national level in Zambia. Here we
aimed to analyze Zambia’s monthly reported passive surveil-
lance MiP data at district-level between 2009 and 2014 and
IPTp data from the Zambian MIS in 2012 to better understand
the burden of MiP, spatial distribution and risk factors of MiP in
the country.
Methods
Study area
Zambia is located in Southern Africa, bordering eight other
malaria-endemic countries that include Angola, Botswana,
Democratic Republic of Congo, Malawi, Mozambique, Namibia,
Tanzania and Zimbabwe.8 In 2014, the population of Zambia
was 13.2 million living within 752 614 km 2 with a population
density of 20 persons per square kilometer.15 Population at the
district level for 2010 was collected from the Central Statistical
Office in Lusaka, Zambia and projected for 2009 and 2011–
2014 based on the 2000 and 2010 national censuses.16,17 While
the country is considered stable politically and economically, it is
also a low-income country with the average GNI per capita of
3810 USD (2013) and 60% of its population living in poverty
(2010).18 The average life expectancy in 2012 was 57 years.18
Zambia is stratified into three malaria epidemiological zones:
stable transmission in the southeastern region of the country
(parasite prevalence of .30%); unstable transmission in the
northeastern and northwestern regions (parasite prevalence of
20%); and low-transmission in the southwestern region (parasite
prevalence ,5%).8 Zambia has a tropical climate with three sea-
sons: rainy season (November to May during which time malaria
transmission peaks); cool, dry season (late May to August); and
hot, dry season (September to November). Malaria prevalence is
highest during the rainy season, however, malaria transmission
occurs throughout the year.4 Plasmodium falciparum is the dom-
inant malaria parasite species (about 98%) in the country.19
2
Sources of data based on collection done between 2009
and 2014
Monthly district-level, aggregated malaria cases (count data)
from January 2009 to December 2014 among pregnant women
were obtained from the Zambian District Health Information
System (DHIS). DHIS data were collected at all heath facilities
including public, private, faith-based hospitals, antenatal clinics,
and rural health centers, in paper form and sent to the District
Health Office (DHO). The date of visit and results of malaria diag-
nosis among MiP were entered in an electronic database at DHO
and transmitted to the provincial office for further processing and
aggregation by the province. The consolidated provincial data
were then transmitted to the NMCC.
District level aggregated data on IRS coverage were collected
from the daily spray forms that were totaled for each year by the
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NMCC. Annually, LLIN coverage data at the district level were
aggregated from various distribution channels such as antenatal
and under-five health clinics, and mass vaccination campaigns.
The life span of the LLINs was assumed to be 3 years.20
A confirmed diagnosis was determined if either a rapid diag-
nostic test (RDT) or thick smear microscopy results were positive.
All RDTs used at the time were WHO recommended RDTs, where
sensitivity and specificity were measured referencing to micros-
copy as gold standard. The RDT brands used in health care facil-
ities throughout the country were either the SD Bioline brand from
Standard Diagnostics, Republic of Korea (sensitivity of 85% [95%
CI, 80–90%]) or SD Bioline Ag-Pf /pan brand (sensitivity of 88%
[95% CI, 83–92%]).21 Unconfirmed diagnoses (i.e., clinical diagno-
ses) were based on clinical case presentation (e.g., headache,
fever, sweating, chills and joint pains)22,23 and without confirm-
ation using microscopy or RDTs. We analyzed MiP in our study
including confirmed and unconfirmed cases.
Malaria prevention, diagnosis and treatment
of pregnant women
Information regarding IPTp was obtained from the 2012 Zambian
MIS.24 In Zambia, during the first trimester of pregnancy, oral
quinine was recommended for malaria treatment among preg-
nant women. In the absence of quinine, artemether-lumefantrine
(AL) was the prescribed treatment.3 During the second and third
trimester, use of artemisinin-based combination therapy (ACT),
specifically AL, was the preferred treatment.3 SP was also the
medicine of choice for IPTp (3 tablets) recommended monthly
after quickening (i.e., 16 weeks following the last menstrual
cycle). The same adult treatment dose of SP (3 tablets) was
recommended monthly (at least 4 weeks apart) during the
second and third trimesters at every scheduled ANC visit. The
total number of doses recommended for the entire duration of
pregnancy was three or more doses.3
Spatial data
Spatial data, including district boundary, geo-coded locations of
Zambia’s 1426 health facilities, lakes, rivers, roads and railroad, were
collected (updated until 2012) from the Ministry of Environment and
Natural Resources. Distances were calculated from the centroid of
each district to the nearest road/rail station and categorized as
follows: ≤2 km¼good access; .2 km¼limited access.
Transactions of the Royal Society of Tropical Medicine and Hygiene

Statistical analysis
Negative binomial regression analysis was completed to investi-
gate the association at district level between the variables for vec-
tor control tools (e.g., LLINs and IRS) and variables for coverage of
health clinics, access to road networks and passenger railways,
and population densities (Table 1). These variables were used to
determine risk factors of MiP. Statistical analyzes were performed
with STATA version 13 (StataCorp, College Station, TX, USA).
Spatial analysis
Yearly maps showing geographic foci of MiP where transmission
intensity exceeds the average level were created for all MiP cases
between 2009 and 2014 using cluster and outlier analysis
(ArcGIS 10.1 software).25 This data was used to make comparisons
of MiP rates within districts, between nearest adjacent districts and
among all districts combined. The test statistic, local Moran’s index
(I), a z-score, p-value, and outlier type were then calculated. Outlier
analysis tool classifies spatial outliers. To ensure this, the tool com-
putes a local Moran’s I value, a z-score, a p-value, and a code (high/
low) representing the cluster form for each feature (based on
weighted features). The z-scores and p-values characterize the
statistical significance of the calculated index values. Here outlier
types indicated whether the values observed between two neigh-
boring foci are more similar (a spatial clustering of either high or low
values) or dissimilar (a spatial outlier) than would be expected at
random. An alpha level of 0.05 was used to determine if the spatial
statistic was statistically significant.
Results

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In Zambia, only 1.5% (398 104 of 28.3 million malaria cases) of
malaria cases reported between 2009 and 2014 (Figure 1) were
Table 1. Prevalence of malaria in pregnancy (MiP) in Zambia, MiP (Table 1). Confirmed cases increased over the years. MiP fol-
2009–2014 lowed same seasonal peaks during the month of January and
March (Figure 2). High burdens of MiP were observed in districts
located in southeastern Zambia and in districts located in the
Year MiP (n¼451 674) Confirmed Non-confirmed north (Figure 3 & Supplementary Figure 1). Between 2009 and
n (%) MiP (%) MiP (%) 2014, MiP cases were evenly distributed (z-score between 21.65
to 1.65) in 60 of the 72 districts of Zambia (Figure 3). There were
2009 57 331 (1.8) 21 786 (38.0) 35 545 (62.0)
few districts in the southern region that had very low MiP cases
2010 102 344 (2.3) 34 797 (34.0) 67 547 (66.0)
during this time period. Milenge district in northern Zambia was
2011 71 407 (1.6) 33 561 (47.0) 37 846 (53.0)
a stable hotspot (z-score .2.58 in 2010 and 2012).26 Persistent
2012 66 471 (1.4) 35 894 (54.0) 30 577 (46.0)
stable hotspots of MiP (z-score .2.58) were reported in the south-
2013 70 752 (1.3) 38 914 (55.0) 31 838 (45.0) eastern region (Petauke, Mambwe, Katete, Chadiza and Chipata
2014 83 369 (1.4) 55 857 (67.0) 27 512 (33.0) districts) of the country during the entire study period between
2009 and 2012. Districts that had better access to passenger

Figure 1. Malaria in pregnancy (MiP) in Zambia, 2009–2014. From the left axis the bar shows total malaria cases. From the right axis the line shows MiP.
This figure is available in black and white in print and in color at Transactions online.

3
M. Kamuliwo et al.

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Figure 2. Seasonality of malaria in pregnancy in Zambia. This figure is available in black and white in print and in color at Transactions online.

Figure 3. Hotspots of malaria in pregnancy in Zambia. This figure is available in black and white in print and in color at Transactions online.

railways, located closer to large water bodies (e.g., lakes and riv- The results of IPTp usage by pregnant women during their last
ers), (Figure 4) and/or high IRS and LLIN coverage, had signifi- birth (in the previous five years), based on the 2007 DHS survey,
cantly lower MiP compared with other districts (Table 2). showed that most pregnant women (85%) reported taking an

4
Transactions of the Royal Society of Tropical Medicine and Hygiene
Figure 4. Map of health facilities, roads, railway lines and water bodies in Zambia. This figure is available in black and white in print and in color at
Transactions online.
antimalarial drug for prevention during their last pregnancy and
71% took two or more doses of IPTp. Regional variations were
observed. Pregnant women living in the Copperbelt (85%) and
Eastern (85%) Provinces, where malaria prevalence is higher than
the national average, had higher rates of receiving two doses of
IPTp during pregnancy as compared to pregnant women in the
Southern (57%), Muchinga (54%) and Western (61%) Provinces
and where malaria prevalence rates are lower than the national
average. Over half of all pregnant women in the country (52%)
reported taking three or more doses of IPTp during their last
pregnancy.
Downloaded from http://trstmh.oxfordjournals.org/ at OUP site access on July 10, 2015
Discussion
Approximately 1.5% of the total number of malaria cases
reported in Zambia between 2009 and 2014 were MiP. There
was a noted increase in confirmed MiP cases during this study per-
iod, with seasonality observed. Districts having access to railways,
waterbodies and greater coverage of IRS and LLINs were asso-
ciated with lower MiP.
Using Zambian DHIS data, the results of this study indicate
that malaria prevalence among pregnant women continues
to be an issue. However, based on these findings, the prevalence
5
M. Kamuliwo et al.

of MiP (1.47%) in Zambia were much lower than the country’s
overall malaria prevalence of 36% (4 738 375 yearly malaria
cases on an average from 2009–2014 of Zambian with 13.2
million people).10 This study also confirmed that MiP is lower
in Zambia than in other African countries such as Malawi,27
Sudan,28,29 Kenya, Mali30 and Gabon.31,32
Despite Zambia being a highly malaria endemic country, per-
sistent and stable hotspots of MiP have been reported only in
Table 2. Risk factors of malaria in pregnancy (MiP) in Zambia,
2009 to 2014
Risk factor PRR (95% CI)
the northeastern part of the country in Milenge district and in
the southeastern region of the country including the Chadiza,
Chipata, Katete, Mambwe and Petauke districts which falls within
the high transmission region of the country.8 Regularly updated
MiP and risk maps33–45 using geographic information systems
will help the NMCC in better control efforts.
This study found that transportation networks, particularly
access to passenger railways and developed roads, and proximity
to large bodies of water within the district were associated with
reduced MiP. One reason for this association might be that
these districts have better and faster access to healthcare
services.
Findings from this study also support a previous study in those
districts with better LLIN coverage contributed to lower MiP preva-
lence.8 A cross-sectional study on the use of LLINs in stable
malaria hotspots among pregnant women would be useful to

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Number of health facilities reporting MiP cases 0.99 (0.97–1.00)
determine the impact of malaria control interventions on MiP.
Population density 1.00 (0.99–1.00)
The association between IRS coverage and MiP was intuitive.
Access to passenger railroad in each district
The results of this study would indicate that consideration for
No 1
focal spraying of houses, particularly along the Malawi and
Yes 0.71 (0.56–0.93) Mozambique borders where malaria prevalence was highest,
Proximity to large bodies of water in each district may contribute in further reducing MiP.10
No 1 In Zambia, IPTp intake increased in 2012 compared with previ-
Yes 0.77 (0.61–0.98) ous years, most notably 2006, 2008 and 2010.7,24 According to the
Access to formal roads in each district DHS data for sub-Saharan African countries between 2007 and
Good access 1 2011, Zambia had the highest rate (66%) of women who received
Limited access 1.40 (1.12–1.77) the recommended two or more doses of IPTp (SP) than any other
IRS (Total houses sprayed in a district in 0.98 (0.98–0.99) sub-Saharan country, with a pooled, weighted average of 20%.46
each year) Detailed documentation47,48 of efficacy and the benefits of IPTp
LLINs (per two household residents coverage) with different antimalarial drugs49,50 could help formulate new
,1 1 policies for MiP. One study based in Zambia in Mansa, the capital
.1 0.43 (0.41–0.44) of the Luapula Province in the northeastern region of the country,
conducted between 2010 and 2011, found a high failure rate of SP
IRS: indoor residual spraying; LLIN: long-lasting insecticide-treated among pregnant women (26%, 15/58).49 The increasing resistance
net; PRR: prevalence rate ratio. of Plasmodium falciparum to SP has heightened concern; this could
explain the persistence of hotspots.

Table 3. The use of intermittent preventive treatment (IPTp) in pregnant women presented by region for Zambia between 2009 and 2014a

Province Percentage of mothers Percentage of mothers who Percentage of mothers who

who took any IPTp took 2+ doses of IPTp took 3+ doses of IPTp

Central 88.7 74.3 51.3

Copperbelt 94.9 85.3 72.6
Eastern 94.9 85.4 68.1
Luapula 89.7 76.6 57.5
Lusaka 94.0 75.1 60.1
Muchinga 72.0 53.5 32.2
Northern 89.7 74.4 53.5
North-Western 79.8 62.1 39.6
Southern 80.1 56.9 36.5
Western 70.6 61.4 46.2
Average 85.4 70.5 51.8

IPTp: intermittent preventive treatment in pregnancy.

a
Based on the last birth (within the 5 years preceding the 2007 Malaria Indicator Survey). This table shows the percentage of pregnant women
who received antimalarial during the pregnancy and the percentage of pregnant women who received IPTp during an antenatal care visit.

6
Transactions of the Royal Society of Tropical Medicine and Hygiene
This study has several limitations that accompany ecological
level analyses. Not all MiP cases were confirmed by either micros-
copy or RDT. Both RDT and microscopy have limited sensitivity and
specificity (by their inability to detect sub-patent malaria parasite
thresholds) which impacts the number of MiP cases identified in
this study. There is a potential for reporting bias due to the vari-
ation in level of accuracy in reporting within different district
levels. In addition, there may be an underestimation of true preva-
lence of MiP attributed to a potential misreporting by health cen-
ters. In addition, the different anti-malarial medications used to
treat MiP during this study period were not accessible and there-
fore their impact on MiP could not be analyzed.
Conclusions
Though MiP remains a burden in Zambia, the reduced prevalence
compared to national records displays observable and encouraging
success of the IPTp program, requiring further stringency and opti-
mization. By mapping the distribution of spatial MiP risk, we provide
baseline measures to plan the future requirements for scaling up
essential disease-prevention strategies. Using these findings, inter-
vention efforts could be concentrated in stable hotspots with high
rates of MiP, during malaria transmission season, particularly in
areas where intervention may not always be available.
Furthermore, logistical challenges need to be investigated in
areas with persistent hotspots of MiP and in high transmission
areas to improve access to services and provide continual surveil-
lance to address MiP issues in the different regions of the country.
Supplementary data
Supplementary data are available at Transactions online (http://
trstmh.oxfordjournals.org/).
Authors’ contributions: UH and KK conceived study design and analyzed
data. MK, EC, JL, TAW, VM, WZ, GM, MMI contributed in writing, and drafted
the manuscript. MAE critically revised the manuscript for intellectual
content. All authors read and approved the final manuscript. MK is the
guarantor of the paper.
Funding: This work was funded in part by the Emerging Pathogens
Institute at the University of Florida and the College of Liberal Arts and
Sciences, as part of the University of Florida Pre-eminence Initiative.
Competing interests: None declared.
Ethical approval: Not required.
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