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An Analysis of Pregnancy-Related Mortality in the
KEMRI/CDC Health and Demographic Surveillance
System in Western Kenya
Meghna Desai
1,2
*, Penelope A. Phillips-Howard
3
, Frank O. Odhiambo
4
, Abraham Katana
1
, Peter Ouma
1
,
Mary J. Hamel
2
, Jackton Omoto
5
, Sheila Macharia
6
, Annemieke van Eijk
3
, Sheila Ogwang
4
,
Laurence Slutsker
2
, Kayla F. Laserson
2,4
1 Malaria Branch, KEMRI/CDC Research and Public Health Collaboration, Kisumu, Kenya, 2 Center for Global Health, Centers for Disease Control and Prevention, Atlanta,
GA, United States of America, 3 Department of Clinical Sciences, Liverpool School of Tropical Medicine, Liverpool, United Kingdom, 4 Health and Demographic
Surveillance System Branch, KEMRI/CDC Research and Public Health Collaboration, Kisumu, Kenya, 5 Department of Obstetrics and Gynaecology, Siaya District Hospital,
Ministry of Health, Siaya, Kenya, 6 Office of Population and Health, US Agency for International Development, Nairobi, Kenya
Abstract
Background:
Pregnancy-related (PR) deaths are often a result of direct obstetric complications occurring at childbirth.
Methods and Findings:
To estimate the burden of and characterize risk factors for PR mortality, we evaluated deaths that
occurred between 2003 and 2008 among women of childbearing age (15 to 49 years) using Health and Demographic
Surveillance System data in rural western Kenya. WHO ICD definition of PR mortality was used: ‘‘the death of a woman while
pregnant or within 42 days of termination of pregnancy, irrespective of the cause of death’’. In addition, symptoms and
events at the time of death were examined using the WHO verbal autopsy methodology. Deaths were categorized as either
(i) directly PR: main cause of death was ascribed as obstetric, or (ii) indirectly PR: main cause of death was non-obstetric. Of
3,223 deaths in women 15 to 49 years, 249 (7.7%) were PR. One-third (34%) of these were due to direct obstetric causes,
predominantly postpartum hemorrhage, abortion complications and puerperal sepsis. Two-thirds were indirect; three-
quarters were attributable to human immunodeficiency virus (HIV/AIDS), malaria and tuberculosis. Significantly more
women who died in lower socio-economic groups sought care from traditional birth attendants (p = 0.034), while less
impoverished women were more likely to seek hospital care (p = 0.001). The PR mortality ratio over the six years was 740
(95% CI 651–838) per 100,000 live births, with no evidence of reduction over time (x
2
linear trend = 1.07; p = 0.3).
Conclusions:
These data supplement current scanty information on the relationship between infectious diseases and poor
maternal outcomes in Africa. They indicate low uptake of maternal health interventions in women dying during pregnancy
and postpartum, suggesting improved access to and increased uptake of skilled obstetric care, as well as preventive
measures against HIV/AIDS, malaria and tuberculosis among all women of childbearing age may help to reduce pregnancy-
related mortality.
Citation: Desai M, Phillips-Howard PA, Odhiambo FO, Katana A, Ouma P, et al. (2013) An Analysis of Pregnancy-Related Mortality in the KEMRI/CDC Health and
Demographic Surveillance System in Western Kenya. PLoS ONE 8(7): e68733. doi:10.1371/journal.pone.0068733
Editor: Thomas Eisele, Tulane University School of Public Health and Tropical Medicine, United States of America
Received December 29, 2012; Accepted May 31, 2013; Published July 16, 2013
This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for
any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.
Funding: HDS S and field staff funding support is acknowledged through individual grants, mainly through The US Presidents Malaria Initiative (PMI), The
President’s Emergency Plan For AIDS Relief (PEPFAR), The Gates Foundation, The European and Developing Countries Clinical Trials Partnership (EDCTP), and the
UK Department for International Development, and through base support from the US Centers for Disease Control and Prevention. Partial funding for this analysis
came from the US Agency for International Development as part of the US government collaboration on the Global Health Initiative.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.
* E-mail: mdesai@ke.cdc.gov
Introduction
Improving maternal health is a high priority for the United
Nations international development agenda. As part of the fifth
Millennium Development Goal (MDG5) set in 2000, maternal
mortality is targeted for substantial reduction by 2015 [1].
Unfortunately, progress in sub-Saharan Africa (SSA) towards this
target has stalled. In 2005, the majority of countries in the region
were estimated to have maternal mortality ratios over 300
maternal deaths per 100,000 live births [2]. Kenya exemplifies
this lack of progress in recent years, with an estimated maternal
mortality ratio of 488 maternal deaths per 100,000 live births
reported for 2008–2009 [3] compared to 414 deaths per 100,000
in 2003 [4]. These estimates translate to approximately 7,700
maternal deaths annually in Kenya.
The leading causes of maternal mortality in SSA are obstetric
complications such as severe bleeding, obstructed labor, infection,
and hypertensive disorders of pregnancy [5]. Major contributors
also include indirect causes such as HIV/AIDS, malaria and
anemia [5,6]. Unsafe abortion, though poorly documented, is also
a major factor which may account for up to 14% of all maternal
deaths worldwide [7]. Many SSA countries would benefit from
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having population based maternal mortality data to prioritize and
better focus interventions to reduce maternal mortality.
Kenya, like many other developing countries, suffers from an
incomplete death registration system and inaccuracy in the
ascertainment of the causes of death, including maternal deaths.
Although studies on maternal mortality have been conducted in
informal settlements [8], there are no published reports of the
causes of pregnancy-related or maternal deaths from rural Kenya.
We utilized verbal autopsy (VA) data collected in the Health and
Demographic Surveillance System (HDSS) site in Nyanza
Province, rural western Kenya to estimate the burden of and
characterize risk factors for pregnancy-related mortality. We also
examined care reportedly accessed by women with a pregnancy-
related death and compared it, where available or appropriate,
with women attributed a non-pregnancy-related death.
Materials and Methods
Study Site and Population
The study site is located in a rural part of Nyanza Province in
western Kenya in the areas of Asembo (Rarieda District), Karemo
(Siaya District) and Gem (Gem District) in Siaya County [9,10].
The population comprises approximately 225,000 individuals
living in 385 villages spread over 700 km
2
. It has a typical rural
African population age distribution with 44.6% under 15 years of
age, and only 5.5% over 65 years of age. By 2008, a total of 94,106
persons were aged 15–49 years, 41.7% of the population, of whom
50,820 (54%) were women of childbearing age. The population is
culturally homogeneous; over 95% are members of the Luo ethnic
community and live through subsistence farming and local
trading. The society is polygynous, with males frequently having
more than one wife, each of whom lives in a separate house with
young children within a single compound. HDSS residents
(defined as those residing in the study area for at least 4
consecutive months or infants born to residents) are visited every
four months. Previous studies identified the population to be
generally very poor [11].
Malaria is endemic in this area, and transmission occurs
throughout the year. The prevalence of malaria among individuals
over 15 years of age ranged between 10–20% in the period 2006
to 2008 (KEMRI/CDC, unpublished observations). HIV, tuber-
culosis (TB) and geohelminth prevalence are also some of the
highest in the country. In the period between 2003 and 2008, in
the HDSS, the prevalence of HIV among girls between 15–19
years of age was estimated at 8.6% [12], the prevalence of TB in
individuals over 15 years of age was 600/100,000 [13], and
geohelminth prevalence in pregnant women was recorded to be as
high as 76.2% [14]. During this time period, HIV treatment and
care centers expanded [15], the coverage of malaria interventions
(insecticide-treated bednets and intermittent preventive treatment
in pregnancy) increased [16], and training of healthcare workers to
provide focused antenatal care was rolled out [17]. There was a
gradual shift in Kenyan policy from allowing traditional birth
attendants (TBAs) to conduct deliveries to redefining their role as
referral agents and birth companions. There are 36 health facilities
in the HDSS, including one district hospital, two privately owned
hospitals, 11 health centers and 22 dispensaries.
Health and Demographic Surveillance System (HDSS)
The entire population is registered and geo-spatially located
within the HDSS [10]. A household census (‘‘round’’) is conducted
three times per year to capture pregnancies, births, deaths, and
internal migration. Socio-economic status (SES), educational and
marriage status data are collected every two years from all HDSS
residents. Demographic data are used to provide mid-year
denominators per 5-year age group, stratified by gender and
study area. Deaths are captured in two ways. First, village
reporters report all deaths to HDSS field supervisors as they occur.
Second, community interviewers record any deaths that occurred
during the prior 4 months at each routine HDSS round. Field staff
then visit the GPS-located coded households at least one month
after the reported death to validate deaths and record events
surrounding death using VA.
Verbal Autopsy (VA)
VAs [18] are administered to the primary caregiver of the
deceased. A standardized questionnaire is used [19], to cover
demographic and personal history, pre-mortem illness signs and
symptoms, and events surrounding the death. VA is conducted for
all deaths. The adult questionnaire is restricted to persons aged 15
years and above. For this analysis, we included women of
childbearing ages: 15 to 49 years. Deaths were linked to HDSS
data including socio-demographic, educational, marital status, and
occupational information. For all deaths, VA information was
reviewed independently and conflicts resolved by at least two
clinical officers (equivalent to physician assistants in the U.S.A.)
and one underlying cause of death assigned. Further details of the
VA methodology used in the HDSS have been provided elsewhere
[20]. Through the year 2007, VA questionnaires asked for
information on miscarriage related to both spontaneous and
induced abortions. In 2008, the standardized WHO VA
questionnaire which only asked women to report induced
abortions was adopted. However, as abortion is illegal in Kenya,
we assume that the data gathered in 2008 predominantly capture
spontaneous miscarriage. VA data are limited in their ability to
differentiate between miscarriage and abortions, thus we do not
present data separately by these categories.
Ethical Considerations
Following cultural customs, compound heads provide written
consent for all compound members to participate in the HDSS
activities. Any individual can refuse to participate at any time. The
HDSS protocol and consent procedures, including surveillance
and VA, are approved by KEMRI and CDC Institutional Review
Boards annually.
Data Handling and Analyses
Data analyzed included all deaths in the HDSS occurring
between January 1, 2003 and December 31, 2008 among female
residents aged 15–49 years at the time of death. Karemo area
(Siaya County), the immediate catchment area of the Siaya
District Hospital, was included in the HDSS in 2008 only. The
following WHO ICD definition of pregnancy-related (PR)
mortality was used: ‘‘the death of a woman while pregnant or within 42
days of termination of pregnancy, irrespective of the cause of death’’. Deaths
were further categorized as either (i) directly PR, where the main
cause of death determined by VA was obstetric, or (ii) indirectly
PR, where the main cause of death ascribed through VA included
any non-obstetric cause: infectious, non-infectious, or external
causes.
Data analyses were conducted using SPSS for Windows
(Release v18.0), and EpiInfo Stat Calc (CDC Atlanta, USA). In
the absence of comparative data among survivors, within-death
comparisons were made between PR and non-PR deaths to
explore differences in characteristics, subdividing analyses into the
WHO grouping of died in pregnancy, died after miscarriage/
abortion, and died within 42 days of pregnancy. Key social and
demographic characteristics included marital status (ever married;
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divorced or widowed at time of death), education (attended and
completed primary school; attended secondary school), SES, and
place of death (home, health facility, hospital, on route to/from
hospital/health facility). A hospital is a district level or above
facility, and a health facility is a local lower level facility. Routinely
collected SES indicators such as occupation of household head,
primary source of drinking water, use of cooking fuel, in-house
assets (e.g. lantern lamp, sofa, bicycle, radio and television) and
livestock (poultry, pigs, donkey cattle, sheep and goats) were used
to calculate a wealth index as a weighted average using multiple
correspondence analysis [21]. This was used to rank households
into wealth quintiles with the first quintile representing the poorest
and the fifth representing the least poor; for some analyses we
collapsed into most (quintiles 1–2) and least (quintiles 3–5) poor.
The significance of changes in rates over time was examined using
Mantel Haenszel x
2
for linear trend. Differences between groups
were determined using Pearson’s x
2
test and Fisher’s Exact test for
small numbers, and a p-value of ,0.05 was considered statistically
significant. The pregnancy-related mortality ratio (PRMR) was
calculated as the number of deaths among women of childbearing
years (15–49 years) over the total number of live births to women
of the same age range per year.
The HDSS data are stored securely and, through a formal
process of data sharing established at KEMRI/CDC, are available
for access to the scientific public two years after the data are
cleaned and frozen.
Results
Comparison of PR and Non-PR Deaths
Between January 1, 2003 and December 31, 2008, 3,223
women aged 15–49 years died in the HDSS; 249 (8%) were
classified as PR deaths. Among all PR deaths, 92 (37%) occurred
during pregnancy, 54 (22%) following a miscarriage, 37 (15%) in
the immediate postpartum period (defined as within 24 hours of
delivery), and 66 (27%) between 1 and 42 days postpartum. Over
half of the PR deaths occurred in women aged 20–29 years,
compared to approximately one-third of non-pregnancy-related
(non-PR) deaths in this age category (Table 1). Almost all (96%) of
PR deaths occurred in women who attended primary school, with
63% completing primary; the proportions who attended or
completed primary education were significantly greater in PR
deaths compared with non-PR deaths (Table 1). Although only
20% of women dying from PR causes attended any secondary
education, this was significantly higher than non-PR deaths (20%
vs. 14%, p = 0.004). Small non-significant variations in PR deaths
occurred by year in comparison to the significant decline in the
number of non-PR deaths observed over the same time period
(Table 1). Marriage at the time of death was significantly higher
among PR compared with non-PR deaths (66% vs. 45%,
p,0.001). Of note, 61% of PR deaths occurred at home and
34% at a health facility or hospital, compared with proportions of
83% and 15%, respectively, among non-PR deaths. Among PR
deaths, a further 6% died on the journey to or from a health
facility. Between 2003 and 2008, there was a trend towards fewer
PR and non-PR deaths occurring in the home (PR deaths: 68% to
46%, p = 0.007; non-PR deaths: 89% to 76%, p,0.001). Lower
SES was significantly associated with a pregnancy-related death
occurring at home (66% in low SES versus 57% in high SES;
p = 0.021).
Estimation of Pregnancy-related Mortality
Figure 1 presents estimates for the PRMR over time and study
area. The total number of live births recorded in the HDSS
between 2003 and 2008 was 34,103, yielding an estimated PRMR
of 740 (95% CI 651–838) per 100,000 live births during the six
year period. The lowest PRMR was in 2005 (524) and the highest
in 2006 (1003) with no overall secular trend (x
2
linear trend = 1.07;
p = 0.3). About one-third (34%) of all PR deaths were due to
directly ascribed (i.e. obstetric) causes, and two-thirds (66%) to
indirect or non-obstetric causes (Figure 2). The obstetric PRMR
was 253 (95% CI 202–313) per 100,000 live births.
Causes of Pregnancy-related Death by Verbal Autopsy
The proportion of PR deaths due to specific direct causes varied
from 31% to 46% during the time period; these changes were not
statistically significant (p = 0.45). The leading causes of direct PR
deaths were postpartum hemorrhage (PPH, 26%), complications
from abortion/miscarriage (17%), and puerperal sepsis (15%)
(Figure 2a). A further 19% of the directly ascribed pregnancy-
related mortality causes was constituted by other complications.
Over one-third (34%) of the PR deaths from a direct maternal
cause occurred within 24 hours of delivery (Table 2). Over 40% of
all PR deaths due to a miscarriage or an induced abortion were in
women aged 25–29 years.
Among all pregnancy-related deaths, HIV/AIDS, malaria, and
TB contributed 30%, 9%, and 6% of deaths, respectively (Table 1).
Among indirect PR deaths, 45% were ascribed to HIV/AIDS,
13% to malaria, and 10% to TB (Figure 2b). Of note, PR deaths
ascribed to HIV/AIDS as the direct cause occurred among
significantly younger women (mean 29.6 years, SD 5.1) compared
with HIV/AIDS ascribed non-PR deaths (mean age 34.3 years,
SD8.3). The majority of indirect PR deaths (43%) occurred during
pregnancy and nine deaths had an undetermined cause (Table 3).
Circumstances Surrounding Pregnancy-related Deaths
Deaths during pregnancy. Of 92 PR deaths that occurred
during pregnancy, the median gestational age at time of death was
5.5 months (SD 2.3), with 26% of women dying in the first, 38% in
the second, and 36% in the third trimester. Nearly two-thirds
(61%) of deaths in pregnant women reportedly had a high fever
before death, and of these, 29%, 45%, and 26% occurred in the
first, second and third trimester, respectively. Vaginal bleeding was
reported in 18 (23%) of 77 deaths during pregnancy where
information was recorded and of these, 30%, 30%, and 40%
occurred in the first, second and third trimester, respectively.
Seizures were reported in 7 (9%) of 76 deaths during pregnancy
where information was recorded; of these 17%, 56%, and 33%
occurred in the first, second and third trimester, respectively. Of
77 pregnancy-related deaths with a record on past complications,
11 (14%) had a history of a previous complicated delivery. A
higher proportion of these women died later in pregnancy (x
2
linear trend = 6.7, p = 0.01), with 10% of these deaths occurring in
the first, 30% in the second and 60% in the third trimester.
Subjectively described ‘‘high fever’’ before death during pregnan-
cy declined from 94% of deaths in 2003, to 30% by 2007 (x
2
linear
trend = 11.0, p = 0.001). The new form in 2008 did not record this
data. There was no difference in the frequency of reported high
fever among pregnant women who reportedly died from an
infectious disease, compared with other causes.
The reported symptom of ‘‘vaginal bleeding’’ during pregnancy
(which was differentiated from peripartum hemorrhage) (n = 18)
was associated with older age, with only four women below 30
years (p = 0.004) reporting this symptom; 29% of vaginal bleeding
occurred in the first, 30% in the second, and 41% in the third
trimester of pregnancy. A third of women who reported to have
had a vaginal bleeding had a history of past delivery complica-
tions, compared with 9% of other pregnancy deaths (p = 0.01).
Pregnancy-Related Mortality in Western Kenya
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Table 1. Distribution of pregnancy-related and non-pregnancy-related deaths of women 15–49 years by socio-demographic and
health-related characteristics.
a
Pregnancy-Related Deaths
All Pregnancy-
Related Deaths
All Non- Pregnancy-
Related Deaths x
2
p value
Post-partum
During
Pregnancy
After
Miscarriage/
Abortions
b
,
24 hrs 1–42 days
n = 92 n = 54 n = 37 n = 66 N = 249 N = 2974
Age at death 15–19 7 (7.6) 1 (1.9) 6 (16.2) 13 (19.7) 27 (10.8) 136 (5.1) 18.27 ,0.001
20–24 25 (27.2) 10 (18.5) 8 (21.6) 19 (28.8) 62 (24.9) 415 (14.8)
25–29 23 (25.0) 22 (40.7) 8 (21.6) 15 (22.7) 68 (27.3) 634 (21.8)
30–34 20 (21.7) 10 (18.5) 3 (8.1) 12 (18.2) 45 (18.1) 532 (17.9)
35–39 9 (9.8) 6 (11.1) 7 (18.9) 6 (9.1) 28 (11.2) 438 (14.5)
40–44 8 (8.7) 4 (7.4) 4 (10.8) 1 (1.5) 17 (6.8) 435 (14.0)
45–49 0 (0.0) 1 (1.9) 1 (2.7) 0 (0.0) 2 (0.8) 384 (12.0)
SES (MCA)
c
(poorest)1 21 (23.9) 11 (22.4) 7 (22.6) 17 (27.0) 56 (24.2) 600 (21.6) 5.13 0.274
2 16 (18.2) 8 (16.3) 5 (16.1) 14 (22.2) 43 (18.6) 583 (21.0)
3 20 (22.7) 11 (22.4) 7 (22.6) 8 (12.7) 46 (19.9) 595 (21.4)
4 13 (14.8) 7 (14.3) 5 (16.1) 12 (19.0) 37 (16.0) 532 (19.2)
5 18 (20.5) 12 (24.5) 7 (22.6) 12 (19.0) 49 (21.2) 464 (16.7)
Area of residence Asembo 34 (37.0) 19 (35.2) 12 (32.4) 25 (37.9) 90 (36.1) 1175 (39.5) 1.11 0.574
Gem 53 (57.6) 35 (64.8) 19 (51.4) 36 (54.5) 143 (57.4) 1624 (54.6)
Karemo
d
5 (5.4) 0 (0.0) 6 (16.2) 5 (7.6) 16 (6.4) 175 (5.9)
Attend Primary Yes 61 (95.3) 36 (100) 26 (92.9) 44 (95.7) 167 (96.0) 1406 (82.9) 20.20 ,0.001
No 3 (4.7) 0 2 (7.1) 2 (4.3) 7 (4.0) 290 (17.1)
Complete Primary Yes 40 (62.5) 25 (69.4) 17 (60.7) 27 (60.0) 109 (62.6) 709 (41.8) 27.85 ,0.001
No 24 (37.5) 11 (30.6) 11 (39.3) 19 (40.0) 65 (37.4) 987 (58.2)
Attend Secondary Yes 19 (21.3) 16 (30.8) 4 (11.4) 9 (14.8) 48(20.3) 329(13.5) 8.18 0.004
No 70 (78.7) 36 (69.2) 31 (88.6) 52 (85.2) 189 (79.7) 2111 (86.5)
Year of death 2003 13 (14.1) 19 (35.2) 5 (13.5) 7 (10.6) 44 (17.7) 568 (19.1) 14.77 0.011
2004 16 (17.4) 12 (22.2) 2 (5.4) 12 (18.2) 42 (16.9) 557 (18.7)
2005 9 (9.8) 5 (9.3) 6 (16.2) 6 (9.1) 26 (10.4) 512 (17.2)
2006 25 (27.2) 10 (18.5) 6 (16.2) 11 (16.7) 52 (20.9) 440 (14.8)
2007 11 (12.0) 4 (7.4) 5 (13.5) 11 (16.7) 31 (12.4) 375 (12.6)
2008 18 (19.6) 4 (7.4) 13 (35.1) 19 (28.8) 54 (21.7) 522 (17.6)
Married at death Yes 60 (65.2) 29 (53.7) 31 (83.8) 43 (65.2) 163 (65.5) 1149 (44.5) 40.06 ,0.001
No 32 (34.8) 25 (46.3) 6 (16.2) 23 (34.8) 86 (34.5) 1432 (55.5)
Place died Home 56 (60.9) 37 (68.5) 20 (54.1) 38 (57.6) 151 (60.6) 2149 (83.0) 88.24 ,0.001
To/from HHF 7 (7.6) 0 (0.0) 3 (8.1) 4 (6.1) 14 (5.6) 38 (1.5)
HF 12 (13.0) 2 (3.7) 6 (16.2) 9 (13.6) 29 (11.6) 146 (5.6)
Hospital 17 (18.5) 15 (27.8) 8 (21.6) 15 (22.7) 55 (22.1) 235 (9.1)
Other 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 20 (0.8)
Distance to HF
e
0–1000 m 19 (20.7) 6 (11.1) 3 (8.1) 14 (21.2) 42 (16.9) 601(20.2) 3.97 0.41
1001–2000 m 37 (40.2) 14 (25.9) 14 (37.8) 22 (33.3) 87 (34.9) 945(31.8)
2001–3000 m 26 (28.3) 21 (38.9) 13 (35.1) 22 (33.3) 82 (32.9) 1051(35.3)
3001–4000 m 10 (10.9) 13 (24.1) 7 (18.9) 5 (7.6) 35 (14.1) 343 (11.5)
4001–5000 m 0 (0) 0 (0) 0 (0) 3 (4.5) 3 (1.2) 25 (0.8)
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Women with vaginal bleeding during pregnancy were more likely
to die at or on route to hospital or a health facility than women
who had no reported history of vaginal bleeding during pregnancy
(p = 0.02), with half dying in the hospital.
Seven women who died during pregnancy had recorded
seizures across all trimesters, with none in the 9
th
month. Seizures
occurred across ages and socio-economic groups, with half
reported in 2006–2007. All but one case died at home. Eclampsia
was defined as the cause of death by VA for 2/7 (29%). In the
remaining women whose deaths were associated with seizures and
who died during pregnancy, the cause of death defined by VA was
TB (1 death), HIV (2 deaths), asthma (1 death) and dysentery (1
death).
Women who died following a miscarriage/abortion. 54
deaths were associated with miscarriage; reported deaths associ-
ated with miscarriages dropped significantly over time (x
2
linear
Table 1. Cont.
Pregnancy-Related Deaths
All Pregnancy-
Related Deaths
All Non- Pregnancy-
Related Deaths x
2
p value
Post-partum
During
Pregnancy
After
Miscarriage/
Abortions
b
,
24 hrs 1–42 days
n = 92 n = 54 n = 37 n = 66 N = 249 N = 2974
HIV/AIDS as cause 23 (25.0) 28 (51.9) 2 (5.4) 21 (31.8) 74 (29.7) 1382 (46.5) 46.6 ,0.001
Malaria as cause 14 (15.2) 3 (5.6) 0 (0) 5 (7.6) 22 (8.8) 178 (6.0) 15.8 0.003
TB as a cause 9 (9.8) 2 (3.7) 1 (2.7) 4 (6.1) 16 (6.4) 458 (15.5) 16.3 0.003
a
Data provided are complete for some variables (gender, age, year death), but for others are not always completed on VA form.
b
Prior to 2008, VA questionnaire asked for all miscarriages (spontaneous or induced). As of 2008, the WHO VA questionnaire was adopted which only asked for induced
abortions.
c
SES (MCA) - socio-economic status (multiple correspondence analysis, in quintiles, 1 = poorest; 5 = least poor).
d
Only generated in 2008.
e
Distance to nearest health facility.
doi:10.1371/journal.pone.0068733.t001
Figure 1. Pregnancy-related mortality ratio in women 15–49 years by year of death and area.
doi:10.1371/journal.pone.0068733.g001
Pregnancy-Related Mortality in Western Kenya
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Figure 2. Classification of major causes of pregnancy-related deaths. A. Directly Ascribed Pregnancy-Related Mortality Causes B. Indirectly
Ascribed Pregnancy-Related Mortality Causes.
doi:10.1371/journal.pone.0068733.g002
Table 2. Distribution of direct causes of death by phase of pregnancy.
Died in
Pregnancy
Died after
miscarriage/abortion
Died within 24
hours after delivery
Died 1–42 days
after delivery Total
Abortion/miscarriage 3 (21.4) 10 (71.4) 0 (0.0) 1 (7.1) 14
Antepartum hemorrhage 5 (71.4) 0 (0.0) 1 (14.3) 1 (14.3) 7
Ecclampsia 7 (100) 0 (0.0) 0 (0.0) 0 (0.0) 7
Obstructed labor 1 (16.7) 3 (50.0) 2 (33.3) 6
Other complications pregnancy,
post-partum & delivery
6 (37.5) 3 (18.8) 4 (25.0) 3 (18.8) 16
Postpartum hemorrhage 0 (0.0) 0 (0.0) 20 (90.9) 2 (9.1) 22
Puerperal sepsis 0 (0.0) 1 (7.7) 1 (7.7) 11 (84.6) 13
Total 22 (25.9) 14 (16.5) 20 (23.5) 20 (23.5) 85
doi:10.1371/journal.pone.0068733.t002
Pregnancy-Related Mortality in Western Kenya
PLOS ONE | www.plosone.org 6 July 2013 | Volume 8 | Issue 7 | e68733
trend = 5.0, p = 0.03), with over half (57%) having been reported
in 2003/2004 and ,15% in 2007/2008. Thus, the contribution of
miscarriages/abortions to PR deaths fell from 43% in 2003 to 7%
in 2008 (Figure 3). Of note, a change in the VA questionnaire in
2008 limited the VA recording of miscarriages when they were
induced. Although miscarriage/abortion associated deaths oc-
curred across all age groups, the highest proportion (40%) of
miscarriages/abortions was among women 25–29 years. The
mean number of reported days until death occurred following
miscarriage/abortion was 16 days (SD 27; range 1–90 days), with
70% of deaths occurring within one week of the miscarriage/
abortion. HIV/AIDS was attributed as the direct cause of death in
52% of all miscarriages/abortion, with a further 6% and 4%
associated with malaria and TB, respectively. Reportedly, 10% of
miscarriages/abortions had been induced; among these, none
were married at the time of death, compared with 60% of women
Table 3. Distribution of indirect causes of death by phase of pregnancy.
Died in
Pregnancy
Died after
miscarriage/abortion
Died within 24
hours after delivery
Died 1–42 days
after delivery Total
HIV 23 (31.1) 28 (37.8) 2 (2.7) 21 (28.4) 74
Malaria 14 (63.6) 3 (13.6) 0 (0.0) 5 (22.7) 22
TB 9 (56.3) 2 (12.5) 1 (6.3) 4 (25.0) 16
Anemia 6 (40.0) 2 (13.3) 3 (20.0) 4 (26.7) 15
Other Infections 6 (46.2) 2 (15.4) 0 (0.0) 5 (38.5) 13
Other [non-infectious] causes
a
8 (53.3) 2 (13.3) 1 (6.7) 4 (26.7) 15
Undetermined 4 (44.4) 1 (11.1) 1 (11.1) 3 (33.3) 9
Total 70 (42.7) 40 (24.4) 8 (4.9) 46 (28.0) 164
a
Other [all other non-infectious causes] (15) = liver (1), CVD (2), injurie s (3), cancers (2), gastro (2), kidney (1), lung (1), CNS (2), other (1).
doi:10.1371/journal.pone.0068733.t003
Figure 3. Proportion of pregnancy-related deaths by phase of pregnancy and year of death.* *Note - prior to 2008, VA questionnaire
asked for all miscarriages/abortions (spontaneous or induced); as of 2008, the WHO VA questionnaire was adopted which only asked for induced
abortions.
doi:10.1371/journal.pone.0068733.g003
Pregnancy-Related Mortality in Western Kenya
PLOS ONE | www.plosone.org 7 July 2013 | Volume 8 | Issue 7 | e68733
being married who had a miscarriage/abortion that was non-
induced (p = 0.011). Over two-thirds (69%) of deaths associated
with miscarriage/abortion occurred at home.
Postpartum deaths (up to 42 days post-delivery). Of 103
deaths in the postpartum period, 37% died within 24 hours, 68%
died by the end of the first week, and 97% within one month, with
a median of 9 days (range 40) between delivery and death. The
majority of postpartum deaths occurred in younger women, and
only 20% in women over 35 years. Nearly half of postpartum
deaths (45%) were among women in the two lowest SES quintiles.
Half (52%) of all post-delivery deaths were classified as maternal
deaths, 23% were attributed to HIV/AIDS, and the remainder
attributed to nutritional, TB, other infections, malaria, and other
causes. Most deaths that occurred within 24 hours of delivery were
attributed to direct obstetric causes compared to deaths that
occurred at least 24 hours after delivery (82% vs. 33%, p,0.001).
A higher proportion of postpartum deaths that occurred at least 24
hours after delivery were HIV/AIDS related, compared to HIV/
AIDS related deaths in the first 24 hours after delivery (34% versus
5%, p = 0.001).
The majority (89%) of women who died postpartum had
delivered vaginally, 10% were by Caesarian-section, and in 1%
forceps were used. VA-reported labor lasting longer than 24 hours
occurred in 38% of cases and 28% of all labors were considered to
be prolonged. Of postpartum deaths with information recorded on
events in the peripartum period, 42% of the deaths were reported
to have had an obstructed labor, 20% bled heavily before delivery,
and 33% bled heavily after delivery.
Of 77 maternal death reports with known place of delivery,
nearly two-thirds (61%) of women delivered at home. Forty-two
percent of home deliveries and 89% of hospital deliveries were in
women from a higher SES (MCA 3–5). 82% of deliveries
conducted by health professionals were among women in the
higher SES group, while 68% of those delivered by a TBA were in
the aggregated lower SES group (p = 0.02; MCA 1–2). The
proportion of post-partum deaths amongst all PR deaths increased
between 2003 and 2008, both among immediate post-partum, and
for those occurring from 1–42 days (Figure 3).
Of 37 deaths in the immediate (24 hours) postpartum period, 25
had delivery information; 48% delivered at home, and 44%
delivered in a hospital or health facility; 40% of women dying post-
partum were delivered by a health professional, 32% by a TBA,
16% by a relative, and 12% by themselves. Forty-nine out of 66
deaths that occurred 1–42 days in the postpartum period had
information available on who performed the delivery; less than a
third (29%) of deliveries were performed by a health professional
in a hospital or health facility.
Nearly all (91%) of the 22 deaths due to PPH occurred within
24 hours of delivery; over a third (36%) of whom were women
over 35 years. Of the 22 PPH deaths, 14 (64%) died at home; all
within 24 hours. Among 13/14 home deliveries who died of PPH,
where details were given, eight recorded who helped at the
delivery: three had a TBA, in three, only relatives were present,
and two delivered themselves. Thus, among known PPH cases
delivering at home, 63% of the deliveries were conducted by the
patient or relatives.
Birth outcomes among women who died post-
partum.
Among 76 postpartum deaths with birth outcome
recorded, 79% had babies born alive. VA documented 39/57
(68%) of babies had died by the time of follow up; 32% died within
7 days, and 36% died after 7 days. By HDSS follow-up, 21% of
babies were healthy and 11% were not thriving. Significantly more
(85%) babies were born alive among mothers surviving the first
day, compared with 64% of those whose mother died in the first
24 hours post-partum (p = 0.04). A higher proportion of babies
were born alive outside of health facilities compared with in-
facilities (90% versus 58%, p = 0.02).
Care seeking before death among women who died of
pregnancy-related and non-pregnancy-related
causes.
Prior to death, 89% of women classified as PR deaths
sought some type of care outside of the home, compared with 98%
of non-PR deaths (p,0.001). While 73% and 72% of women with
PR and non-PR related causes of death, respectively, sought some
form of hospital care before death, a review of other types of care
sought illustrates significant differences in sources of care among
PR and non-PR deaths: religious leaders (30% versus 39%,
p = 0.004), pharmacy or drug seller (52% versus 71%, p,0.001),
and health facilities (47% versus 58%, p = 0.002). While a higher
proportion of women with a PR death sought help from a TBA
(18%), compared with deaths that were non-PR (15%) this was not
statistically significant (p = 0.19). When separating out women who
died within or after 24 hours of delivery, 54% of those dying
within 24 hours had sought care from a hospital, physician or
health facility, compared with 89% of women who died later post-
partum (p,0.001).
SES was not associated with health seeking in general; however
differences were evident by type of care sought. Thus, while 25%
overall visited a traditional healer, the proportion increased as SES
decreased, with 31% visiting traditional healers in the lowest MCA
quintile compared with 16% in the highest (x
2
linear trend 4.2,
p = 0.04). Similarly, 34% of the poorest sought care from TBAs
compared with 12% in the highest MCA quintile (x
2
linear
trend = 4.5, p = 0.034). The reverse was evident for hospital care,
with 90% of women in the highest MCA quintile seeking hospital
care compared with 60% in the lowest (x
2
linear trend = 11.4,
p = 0.001).
Discussion
During the six year period between 2003 and 2008, we
estimated a pregnancy-related mortality ratio of 740 (95% CI
651–838) per 100,000 live births within the KEMRI/CDC Health
and Demographic Surveillance System in Nyanza Province,
western Kenya with no evidence of reduction over time. If we
remove all incidental or accidental causes of death as ascribed by
VA, as well as deaths due to undetermined causes, the resulting
maternal mortality ratio is 669 (95% CI 584–762) per 100,000 live
births. This estimate is higher than the national estimate of 488
(95% CI: 333–643) per 100,000 live births reported by the Kenya
Demographic and Health Survey in 2008/2009 for approximately
the same time period, and far above the national target of 147 per
100,000 by 2012 [22]. The lifetime risk of dying from pregnancy-
related causes in the HDSS was 1 in 26, in contrast to over 1 in
7300 for women from developed countries, underscoring a very
large inequity in maternal mortality [6].
Nearly one-third of deaths were due to direct obstetric causes.
Postpartum hemorrhage was the leading obstetric cause of death,
which is likely a direct reflection of the lack of access to timely and
competent hospital care. Most women who died of PPH delivered
at home, where essential skills and interventions (misoprostol and
safe blood) are not available, and timely transfer to health facilities
during a time of obstetric emergency is difficult. The majority of
peripheral health facilities in the HDSS also lack misoprostol, safe
blood, and appropriate septic techniques to manage the leading
causes of obstetric complications in this area (Sheila Ogwang,
personal communication). Complications associated with abor-
tion/miscarriage were also a common direct cause of PR deaths,
and all of these deaths were in unmarried women. Data from
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ongoing studies in the HDSS suggest that 80% of pregnancies are
unintended [23]; 75% of women of childbearing age in this area
do not have access to family planning (HDSS, unpublished data),
compared to the national [3] and SSA [24] estimate of 25%. This
gap can largely be attributed to inadequate service provision,
unreliable access to family planning commodities and limited
resource allocation nationally. Furthermore, unmarried females
may have difficulty accessing ‘family planning’ because contra-
ceptives may be considered only appropriate for married women
[25]. In this context, improved access to family planning
commodities and implementation of interventions to reduce the
risk of death posed by unintended pregnancies and unsafe
abortions [7] should be considered.
Among pregnancy-related deaths recorded in this study, only
33% were delivered by a skilled birth attendant (health worker
with midwifery skills). Nationally, the proportion of births
managed by health professionals and the proportion delivered in
a health facility are 44% and 43%, respectively [3]. Skilled birth
attendance in the HDSS has improved from 17% in 2002 [26] to
39% in 2010 (KEMRI/CDC, unpublished data), most likely as a
result of policy changes and maternal health initiatives to improve
access to and removal of barriers for the use of skilled birth
attendants. This improvement in skilled birth attendants, however,
fell short of the global target of 85% skilled birth attendants for
2010 [27].
There was no difference in seeking care from a TBA between
PR and non-PR deaths, which implies that in this community,
TBAs may be providing care to both pregnant and non-pregnant/
non-parturient women. Furthermore, women of lower socioeco-
nomic status were more likely to deliver at home and less likely to
seek care from a health facility any time before their death. A
program that encourages TBAs to accompany women in labor to
the health facility from their community, and allows TBAs to
provide emotional support during labor and delivery may increase
skilled birth attendance and improve maternal and perinatal
outcomes in rural Kenya [28,29], while still involving these
important community members. Furthermore, closing the gap on
availability of and access to facilities offering emergency obstetric
care (EmOC), along with targeted health education and support
during pregnancy, improvements in the transport and communi-
cation referral network, and provision of free high quality
maternity services should also help with realization of the
MDG5 goals in this area. These changes should ideally be
accompanied by a systematic evaluation of the quality of care
provided to women presenting to health facilities for delivery.
Efforts to improve skilled birth attendance in the HDSS have been
accelerated since 2010. Only 5 (14%) of the 36 health facilities in
the HDSS provided some level of EmOC in 2002, and after nearly
a decade of multiple efforts to improve skilled birth attendance, 2
(6%) offered comprehensive EmOC, one quarter (9 facilities)
offered the full spectrum of basic EmOC services, and 21 offered
some level of basic EmOC (missing one or more of the key
services); while 4 did not offer any obstetric care services by the
end of 2011 (Sheila Ogwang, personal communication).
Almost one-third of the pregnancy-related deaths that occurred
in a health facility or hospital had delivered at home, providing an
example of the ‘‘Three Phases of Delay Model’’ [30]: delay in
recognition of illness, delay in seeking and accessing care, and
delay in the provision of care once at a health facility. Family
influence, cost and poor healthcare staff attitude have been cited as
reasons why women do not seek facility-based delivery services in
this area [31]. Poor road infrastructure and lack of functional
ambulatory services further hinders referrals and access to EmOC.
Our data also suggest that women who are successful in reaching
the health facility for a delivery should be kept under observation
for at least 24 hours following the delivery, as one-third of the
pregnancy-related deaths from a directly attributable cause occur
within that period.
According to VA findings, nearly two-thirds of deaths were due
to indirect, non-obstetric causes. This contrasts to a recent WHO
analysis on maternal deaths in Africa which suggests that the
majority of deaths are due to direct obstetric complications around
the time of childbirth [5]. Our study is in agreement with an
autopsy study of maternal mortality at a tertiary health facility in
Mozambique which highlights the importance of infectious causes
of maternal death [32]. In our study, HIV/AIDS, malaria, TB
and anemia accounted for 30%, 9%, 6% and 6% of all pregnancy-
related deaths, respectively [33,34,35]. TB in association with
HIV/AIDS is increasingly recognized as a major contributor to
maternal mortality in SSA [36]. Our findings suggest an
opportunity to implement a streamlined program of integrated
point-of-care detection and appropriate management of these
major pregnancy-related illnesses in a setting where 92% of
pregnant women attend at least one antenatal care visit [3]. It also
highlights the need to improve access to and increase uptake of
prevention and treatment measures against these infections.
According to the VA, malaria was a significant ascribed cause of
pregnancy-related death (65 per 100,000 live births). These data
add to the scarcity of literature documenting the impact of malaria
on maternal mortality in Africa [37]. It has commonly been
assumed that malaria in pregnancy is associated with death
predominantly in areas of unstable or low malaria transmission
[32,38]. However, an earlier review suggests that the overall
percentage of maternal deaths attributed to malaria from direct
and indirect causes in low transmission areas outside of Africa
(0?6–12?5%) is not substantially different from the estimate derived
for high transmission areas (0?5–23?0%) [39]; our data support this
finding. Within the study area in past years, interventions have
been conducted to reduce the harmful effects of malaria in
pregnancy, specifically with insecticide-treated bednet distribution
for pregnant women [40], intermittent presumptive treatment with
sulfadoxine-pyrimethamine [41,42], and training of healthcare
workers to provide focused antenatal care [17]. However,
assessments of outcomes from these interventions have generally
focused on the impact on low birth-weight and neonatal mortality,
but not on reduction in pregnancy-related mortality. More data
are required in determining the effect of these and other antenatal
care interventions on maternal survival.
Our evaluation was subject to several limitations: 1) In the
absence of linkage to antenatal care data, we were unable to fully
ascertain the health status of pregnant women before they died; 2)
The small number of pregnancy-related deaths resulted in wide
confidence intervals and likely contributed to substantial fluctua-
tions in annual estimates of pregnancy-related mortality. Future
analyses over longer time periods should allow for more precise
estimates as well as evaluation of the impact of current
interventions on maternal mortality; 3) Since national estimates
are not disaggregated by province or even rural/urban settings, we
are unable to make any comparisons at that level; however, our
data contribute much needed sub-national mortality information
to prioritize interventions [43]; 4) Of all deaths, over 90% are
followed up with VA in the community, the remaining not being
followed due to migration, absence of an adult or next of kin at the
time of household visit. VA is expected to underestimate
pregnancy-related deaths by about 15% [44] due to recall bias
and the absence of diagnostics. Furthermore, questioning of
symptomatology around obstetrical complications is particularly
difficult, and likely misses a number of clinical signs not witnessed
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PLOS ONE | www.plosone.org 9 July 2013 | Volume 8 | Issue 7 | e68733
by relatives or other respondents. This potentially under-estimates
some symptomatology around PR deaths, limits our interpretation
of clinical events, and prevents chronological evaluation of events
leading up to the time of death. In most SSA countries, including
Kenya, pregnancies are not declared early [43] which further
reduces the likelihood of capturing all pregnancy-related deaths
through VA. That the majority of miscarriages/abortions and
post-partum deaths were classified under other causes raises our
suspicion that mortality from this cause is under-reported. In
addition, cultural factors appear to act as a strong barrier against
disclosure of miscarriage in the HDSS community (Stephanie
Dellicour, personal communication); 5) Changes in the verbal
autopsy questionnaire on miscarriage in 2008 may have also
reduced ascertainment in that year, thus this may have exagger-
ated the proportionate fall in miscarriage, relative to other indirect
causes. Further, legalities surrounding induced abortion likely also
influenced accurate reporting of such events; 6) We recognize
within-death comparison reflects behaviors of selected sub-
populations, but for many variables no comparative data were
available among healthy deliveries; 7) We did not use the WHO
ICD definition of maternal mortality but instead chose to use its
definition of pregnancy-related mortality which includes deaths
due to incidental or accidental causes. While there is very limited
literature on external causes of death during pregnancy [45,46,47],
and the relationship between pregnancy and such external causes
is likely to be complex and context-specific, we believe that
incidental deaths may, at least in part, be pregnancy-related in
resource-poor settings such as western Kenya where scenarios like
the poor care of a pregnant woman diagnosed with cancer or
domestic violence during pregnancy cannot be underestimated;
and 8) Ascertainment of changing mortality trends depends on a
robust ongoing surveillance system. The HDSS has been in
existence since a large insecticide-treated bednet trial, and
improved with membership into INDEPTH with standardization
of forms to enhance capture of signs and symptoms informing
diagnosis [10]. Since 2003, capture of deaths has been standard-
ized, yet cyclical variations by year are evident; the lower than
expected mortality rate in 2005, followed by a higher rate in 2006
was also documented within other sub-populations in the HDSS;
while no clear explanation for this occurrence is evident, it appears
to be a population level phenomenon rather than maternal-
specific. We recognize verbal autopsy has numerous limitations in
its ability to define cause of death; new approaches to analyzing
symptomatology with classification by WHO ICD-10 codes is
underway, such as the use of a computerized algorithm [48,49]
which is hoped will strengthen future analyses. Despite these
limitations, we believe these data represent unique and robust
information from SSA and contribute to the literature about
events surrounding pregnancy-related mortality.
Conclusions
In a rural area of western Kenya, we observed very high
pregnancy-related mortality, the leading causes of which were
HIV/AIDS, malaria, postpartum hemorrhage, TB, anemia,
miscarriage/abortion, and puerperal sepsis. Data from the HDSS,
and VA identifying underlying causes, suggest most public health
surveillance systems in areas of high disease burden may be
underestimating certain causes of PR deaths. Over two-thirds of
the pregnancy-related deaths identified over the study period were
preventable. Our data also attest to the limited care seeking
currently adopted by women during pregnancy, with substantial
numbers seeking care from traditional practitioners. There is
potential to substantially reduce pregnancy-related mortality in
rural Kenya, and indeed in SSA, by targeting endemic infectious
diseases prior to and during pregnancy, as well as ensuring all
pregnant women have access to good quality antenatal care,
skilled care during delivery, emergency obstetric care as well as
post-natal care. In the past few years, several development
partners and U.S. government organizations across SSA have
allocated limited resources towards maternal health programs.
Our findings show that these efforts need to be targeted towards
improving pregnancy-related and maternal health care both at
home (through community health advocacy and education) and at
health facilities (through improved healthcare worker training,
supervision, and guidelines in provision of antenatal and obstetric
care). It is time to implement and measure the impact of a
targeted, evidence-based approach to reducing pregnancy-related
mortality in Kenya. As one practicing gynecologist and head of a
district hospital in rural western Kenya said, ‘‘No woman should die
while giving forth life’’.
Acknowledgments
Disclaimer: The findings and conclusions in this paper are those of the
authors and do not necessarily represent the views of the Centers for
Disease Control and Prevention.
We are grateful to the communities of Asembo, Gem and Karemo for
their participation in and support of the HDSS. We also thank numerous
field, clinical, data and administrative staff, without whom, this study would
not have been possible. We thank Dr. Isabella Danel, head of the Maternal
and Child Health Group at the Center for Global Health, CDC for
providing invaluable insight and comments for the development of this
manuscript. We thank INDEPTH for their ongoing collaboration to
strengthen and support health and demographic surveillance systems:
KEMRI/CDC Research and Public Health Collaboration is a member of
the INDEPTH Network. This manuscript has been approved by the
Director of KEMRI, and is a product of activities being implemented as
part of the learning agenda of the United States Government’s Global
Health Initiative in Kenya.
Author Contributions
Conceived and designed the experiments: MD PPH KL. Performed the
experiments: FO PPH MD KL. Analyzed the data: PPH FO MD.
Contributed reagents/materials/analysis tools: FO MH AvE PPH MD SO
LS KL. Wrote the paper: MD PPH AK KL. Provided scientific leadership
in developing the HDSS field site and scientific activities: LS KL.
Commented on and edited the manuscript: LS FO AK PO MH SO SM
JO AvE. Developed and supported the VA methodology: FO MH AvE.
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