J HEALTH POPUL NUTR

2007 Sep25(3):328-335 ©INTERNATIONAL CENTRE FOR DIARRHOEAL

ISSN 1606-0997 | $ 5.00+0.20 DISEASE RESEARCH, BANGLADESH

Prevalence and Public-health Significance of HIV

Infection and Anaemia among Pregnant
Women Attending Antenatal Clinics in
South-eastern Nigeria
C.J. Uneke1, D.D. Duhlinska2, and E.B. Igbinedion3
1
Department of Medical Microbiology/Parasitology, Faculty of Clinical Medicine, Ebonyi State University, Abakaliki, Nigeria,
2
Department of Zoology, Faculty of Natural Sciences, University of Jos, Nigeria, and 3Department of Applied Microbiology,
Faculty of Applied and Natural Sciences, Ebonyi State University, Abakaliki, Nigeria

ABSTRACT

HIV infection and anaemia are major public-health problems in Africa and are important factors associated
with an increased risk of adverse pregnancy outcomes. The objective of this study was to determine the
prevalence of HIV infection and anaemia among pregnant women attending antenatal clinics in south-
eastern Nigeria. To achieve this, a cross-sectional survey was conducted during July 2005–June 2006 using
standard techniques. Of 815 pregnant women studied, 31 (3.8%, 95% confidence interval [CI] 2.5-5.1)
were HIV-positive. Maternal age and gestational age were not associated with HIV infection (p>0.05). The
prevalence of anaemia (Hb   <11.0 g/dL) was 76.9%, and 15 (1.8%, 95% CI 0.9-2.7) had severe anaemia
(Hb   <7.0 g/dL). A significantly higher prevalence of anaemia was observed among individuals in their
second pregnancy trimester (p<0.05) and those infected with HIV (p<0.05). Since HIV and anaemia are
preventable, antenatal care services could serve as a pivotal entry point for simultaneous delivery of inter-
ventions for the prevention and control of HIV infection and anaemia in pregnant women.

Key words: Anaemia; Cross-sectional surveys; HIV; HIV infections; Maternal health; Morbidity; Mortality;
Pregnancy; Pregnancy outcomes; Prevalence; Risk factors; Nigeria

INTRODUCTION haran Africa, a high prevalence (95.4%) of anae-

mia has been reported among pregnant women
Despite the considerable improvement in health- (3), with the mean prevalence of maternal anaemia
care-delivery services in many parts of the African
in the subregion estimated to be 61% (4). Anae-
continent, making motherhood safer, which is an
mia even when mild is associated with reduced
urgent priority and one of several child-survival
productivity at work (5). During pregnancy, severe
strategies applied through antenatal care, conti-
anaemia may result in circulatory changes that are
nues to be particularly challenging. Anaemia in
associated with an increased risk of heart failure (6).
pregnancy has been described as one of such enor-
During labour, women with severe anaemia are less
mous medical challenges because it is a major
public-health problem in Africa and is an impor- able to endure even moderate blood loss and, as
tant factor associated with an increased risk of poor a consequence, are at a higher risk of requiring a
pregnancy outcomes (1) and maternal morbidity blood transfusion during delivery (7,8). In addi-
and mortality in developing countries (2). In sub-Sa- tion, severe anaemia in pregnancy is an important
direct and indirect cause of maternal death (9,10),
Correspondence and reprint requests should be and for the foetus, severe maternal anaemia may
addressed to: result in intrauterine growth retardation, stillbirth,
Dr. C.J. Uneke
and low birthweight (11-13).
Department of Medical Microbiology
Faculty of Clinical Medicine The aetiology of anaemia in pregnancy in sub-
Ebonyi State University
Saharan Africa is complex and multifactorial (7).
PMB 053 Abakaliki
Nigeria Apart from malaria, other causes of anaemia in
Email: unekecj@ yahoo.com pregnancy include an iron- and folate-deficient
Fax: 234-04300222 diet and infections, such as hookworm, and in-
HIV infection and anaemia in pregnancy Uneke C.J et al.

creasingly human immunodeficiency virus (HIV) can be evaluated. The public-health implications of
(14). It has been suggested that infection with HIV findings as they affect the overall maternal well-be-
during pregnancy may be associated with an in- ing in this part of the globe are discussed.
creased risk of anaemia-related maternal death in
developing-country settings due to the increasing MATERIALS AND METHODS
severity of anaemia or due to the combined effects Study area
of anaemia and other infections (15). Anaemia also
has been associated with progression of HIV disease This investigation was conducted in two major cit-
(16). Concerning the global HIV epidemic, sub-Sa- ies—Abakaliki, the Ebonyi State capital, and Enugu,
haran Africa remains by far the worst-affected re- the Enugu State capital—in south-eastern Nigeria
gion with 25.4 million people living with HIV (just during July 2005–June 2006. The study settings are
under two-thirds, i.e. 64% of all people living with separated by a distance of about 100 km and have
HIV) (17). The HIV/AIDS epidemic is affecting fe- similar socioeconomic, ethnic and religious charac-
males most severely in the subregion, and women teristics, except that Enugu is a much more deve-
of reproductive age make up almost 57% of adults loped city than Abakaliki, particularly in terms of
living with HIV, accounting for up to 80% of HIV- commerce and industries. Two of the largest hospi-
infected women in the world (17,18), with HIV- tals in the cities—Ebonyi State University Teaching
prevalence rates sometimes exceeding 40% among Hospital (EBSUTH), Abakaliki and Balm of Gilead
pregnant women (19,20). Hospital (BGH), Enugu, which serve as referral cen-
tres for gynaecological services and run the biggest
The HIV/AIDS epidemic intersects with the prob- antenatal clinics, were used for the study.
lem of maternal mortality in many circumstances
in sub-Saharan Africa. The extent of the contribu- Ethical considerations
tion of HIV/AIDS to maternal mortality is difficult
Ethical approval for this study was obtained from
to quantify, as the HIV status of pregnant women
the Faculty of Clinical Medicine (Infectious Diseas-
in the subregion is not always known (21). HIV
es Research Division, Department of Medical Mi-
impacts on direct (obstetrical) causes of maternal
crobiology), Ebonyi State University, Abakaliki, and
mortality by an associated increase in pregnancy-
from the ethical committee of the EBSUTH, Abaka-
related complications, such as anaemia, postpar-
liki and of the BGH, Enugu. Approval was granted
tum haemorrhage, and puerperal sepsis (8,21).
subject to patient anonymity being maintained,
Although anaemia is highly prevalent during
good laboratory practice/quality control being en-
pregnancy and is common during HIV infection,
sured, and every finding being treated with utmost
anaemia and iron status have not been well-char-
confidentiality and for the purpose of this research
acterized in HIV-infected pregnant women in most
only. All work was performed according to the in-
parts of sub-Saharan Africa (22). A relationship be-
ternational guidelines for human experimentation
tween HIV seropositivity and a decreased haemo-
in clinical research (24).
globin (Hb) concentration in pregnancy has been
suggested, and the inclusion of HIV screening in Study population/sampling technique
differential diagnosis of anaemia is recommended
(23). However, the paucity of comprehensive popu- Pregnant women in their various pregnancy trimes-
lation-based data on anaemia and HIV infection in ters who visited the antenatal clinics (ANCs) of the
pregnancy in Nigeria and other parts of West Af- EBSUTH, Abakaliki, and the BGH, Enugu, within
rica with a similar setting makes the formulation the study period, at their first visit to the antenatal
of policies that would transform into effective and care clinic since the commencement of pregnancy
sustainable intervention/control programmes for were considered for the study. All the subjects
pregnant women an enormous challenge to health were verbally notified prior to sample collection,
policy-makers. and their informed consent was duly obtained.
Age of each woman and pregnancy trimester was
This present study was, therefore, designed to pro- determined by interview. A sample of about four
vide scientific information on the prevalence of mL of blood was obtained by venepuncture from
anaemia and HIV infection and associated factors each patient for analysis. For the purpose of the re-
to maternal anaemia, which can be used for direct- search, no personal identifiers (names, ID number,
ing policy development and control-programme address, etc.) were used on the blood sample of
implementation and also provide a baseline mea- the participants. Instead, bar-coded numbers
surement on which the impact of interventions were used for ensuring anonymity of the donors,

Volume 25 | Number 3 | September 2007 329

HIV infection and anaemia in pregnancy Uneke C.J et al.

facilitating laboratory procedures, and minimiz- at the EBSUTH, Abakaliki, where 21 (5.3%, 95% CI
ing the chances of errors during the handling of 3.1-7.5) of 394 individuals screened were infected
the blood specimens. All specimens were analyzed with HIV, while at the BGH, Enugu, 10 (2.3%, 95%
within one hour of collection. CI 0.9-3.7) of 421 pregnant women screened had
HIV infection (Table 1). When maternal age was
Laboratory analysis
associated with HIV infection, the prevalence de-
Blood samples obtained from the subjects at the creased with increase in age. Although individuals
BGH, Enugu, were analyzed at the laboratory unit in the 20 years and less age-category recorded the
of the hospital for haemoglobin (Hb) concentration highest prevalence of HIV infection, the differ-
using the cyanmethaemoglobin method described ence in the trend was not statistically significant
previously (25); reading was done using a spectro- (χ2=2.23, p>0.05). The association of HIV infection
photometer (Bayer RA 50). The packed cell volume with gestational age indicated that the highest in-
(PCV) was determined for samples obtained from fected individuals were more likely to be in their
subjects at the EBSUTH, Abakaliki, using the hae- third pregnancy trimester. However, there was also
matocrit technique (25), at the Research Laboratory no statistically significant difference in the trend
of the Department of Medical Microbiology, Ebo- (χ2=1.71, p>0.05) (Table 1).
nyi State University, Abakaliki. The PCV (%) values
Of the 815 women screened, 15 (1.8%, 95% CI 0.9-
were converted to Hb (g/dL) by applying the con-
2.7) had severe anaemia (Hb <7.0 g/dL). The com-
stant factor of 0.3 (26). The commercially-available
bined prevalence of anaemia (Hb <11.0 g/dL) was
HIV Tri Line Test-kits (Biosystem Inc, Austria) were
first used for screening the serum sample of each 76.9%. A higher prevalence (83.8%) of anaemia
subject which was separated from blood to detect was recorded among the subjects at the EBSUTH,
antibodies to HIV-1 and HIV-2. Thereafter, HIV-se- Abakaliki, than their counterparts at the BGH, Enu-
ropositive samples were confirmed by immunoblot gu (70.5%). The prevalence of anaemia decreased
analysis using the commercially-available BIORAD with age but the difference was not statistically
New Lav Blot-kits (Bio-Rad Novapath Diagnostic significant (χ2=5.06, p>0.05) (Table 2). When ges-
Group, USA). The instructions of the manufacturer tational age was related with anaemia, individuals
were strictly followed to determine the serostatus in their second pregnancy trimester had a signifi-
of the samples. cantly higher prevalence of anaemia than those in
their first and third pregnancy trimesters (χ2=9.24,
Results of both HIV and haemoglobin tests were p<0.05). The prevalence of anaemia was signifi-
made available to all the study participants. All the cantly higher among the HIV-positive women than
pregnant women who were HIV-positive were in- those who were HIV-negative (χ2=7.23, p<0.05)
formed of their HIV status by their physicians and (Table 2). The mean haemoglobin concentration of
were offered counselling and also enrolled into the the HIV-positive women was 8.6 g/dL, while that of
free maternal antiretroviral therapy programme of the HIV-negative women was 10.2 g/dL.
the EBSUTH. Also, all the women after enrollment
at the antenatal clinics of the two hospitals were DISCUSSION
given chemoprophylaxis, including haematinics,
The results of this investigation confirmed the re-
to treat anaemia, particularly for those who were
sults of earlier reports from various parts of sub-Sa-
anaemic.
haran Africa which indicated that the prevalence
Statistical analysis of anaemia among pregnant women is unaccept-
ably high in the region (3-7). Although anaemia in
The 95% confidence interval was calculated using pregnancy in sub-Saharan Africa has multiple aetio-
the standard method. The differences in propor- logies, in countries with a high prevalence of HIV
tion were evaluated using the chi-square test. The infection, anaemia due to underlying nutritional
statistical significance was achieved if p value was deficiencies may be intensified by parasitic infec-
<0.05. tions, compromised immunity, and the haemato-
logical consequences of chronic and systemic in-
RESULTS
flammation (14). In this present investigation, up
In this investigation, a combined total of 815 preg- to 76.9% of the total number of pregnant women
nant women were studied, and 31 (3.8%, 95% studied were anaemic (with Hb <11 g/dL), and HIV
CI 2.5-5.1) of these women were HIV-positive. A infection was a major contributor to anaemia seen
higher prevalence of HIV infection was recorded in pregnancy. These findings are consistent with

330 JHPN
HIV infection and anaemia in pregnancy Uneke C.J et al.

those of some earlier reports (8,15,16,22). A younger

95% CI

0.2-9.4
2.6-6.0
0.1-4.5

2.5-5.1

0.8-5.2
1.3-5.1
2.6-6.6
2.5-5.1
age appeared to be a higher risk factor to both HIV

-
infection and anaemia but the differences were not
statistically significant (p>0.05).
Table 1. Prevalence of HIV infection in relation to age and gestational age among pregnant women attending antenatal care clinics in

The relationship between HIV seropositivity and a

4.8
4.3
2.3
0.0
3.8

2.2
3.2
4.6
3.8
% decreased haemoglobin concentration in pregnan-
Total overall
HIV+ve

cy, which was suggested earlier (23), was confirmed

in the present study. Our results showed that the

BGH=Balm of Gilead Hospital, Enugu; CI=Confidence interval; EBSUTH=Ebonyi State University Teaching Hospital, Abakaliki
prevalence of anaemia was significantly higher
No.

4
23
4
0
31

2
10
19
31
among the HIV-positive women than among the
HIV-negative women (p<0.05), and a lower mean
haemoglobin concentration was recorded among
No. exam-

the HIV-positive women compared to the HIV-

ined

83
541
172
19
815

90
316
409
815
negative women. This was consistent with the
findings of similar studies in Kisumu, Kenya (27),
Harare, Zimbabwe (28), Blantyre, Malawi (22,29),
95% CI

and Bobo-Dioulasso, Burkina Faso (31). The under-

2.7-8.5
0.9-4.9
1.0-3.2

0.9-3.7

1.0-6.4
0.2-3.6
0.4-5.6
0.9-3.7
lying mechanisms by which HIV infection pro-
-

duces anaemia are not fully understood. However,

the suggested mechanisms include a direct effect of
the virus itself (32), bone marrow suppression as a
2.9
2.9
1.1
0.0
2.3

2.7
1.7
3.0
2.3
%

result of cytokine release (33), anaemia as a result

BGH, Enugu
HIV+ve

of chronic inflammation or opportunistic infec-

tion (34), reduced erythropoietin production and
response (35), and deficiency of vitamin B12 or fo-
No.

1
8
1
0
10

2
3
5
10

lates (29). The implication of these findings is that

infection with HIV should be considered a possible
additional aetiologic factor having a significant ef-
No. exam-

fect on haemoglobin levels among pregnant wom-

ined

35
273
94
19
421

74
178
169
421

en even in the absence of evidence of concurrent

opportunistic infection and/or nutritional deficien-
cy. An earlier report suggested that, in areas with a
high prevalence of HIV positivity, studies pertain-
0.6-13.2
95% CI

2.8-8.4
1.6-6.0

3.1-7.5

1.4-8.8
2.8-8.8
3.1-7.5

ing to anaemia and its aetiology should, therefore,

-

include an assessment of HIV status (29).

It is pertinent to note that the apparently high

EBSUTH, Abakaliki

rate of anaemia recorded among the HIV-negative

6.3
5.6
3.8
0.0
5.3

0.0
5.1
5.8
5.3
%

women (76.1%) in this study clearly showed that

HIV+ve

HIV infection was not the only major determinant

of anaemia observed among the subjects. In many
areas of sub-Saharan Africa, including Nigeria, ma-
No.

3
15
3
0
21

0
7
14
21

laria and iron deficiency have been shown to sub-

south-eastern Nigeria

stantially produce anaemia in pregnancy (3,7,11).

In a review of studies of Plasmodium falciparum-re-
No. exam-

lated anaemia in pregnant women, it was suggested

ined

48
268
78

394

16
138
240
394
0

that up to 400,000 pregnant women develop mod-

erate or severe anaemia (Hb <8.0 g/dL or haemato-
crit <25%) each year in sub-Saharan Africa as a re-
sult of malaria infection (30). Thus, in populations
Age (years)
Parameter

Trimester

with a high risk of exposure to infectious diseases,

Second
21-30
31-40

Third
Total

Total

particularly malaria, the vicious cycle of infection,

First
≤20

≥41

impaired immunity, and anaemia may result in a

stronger association between HIV infection and

Volume 25 | Number 3 | September 2007 331

332
Table 2. Prevalence of anaemia in relation to age, gestational age, and HIV infection among pregnant women attending antenatal clinics in
south-eastern Nigeria

EBSUTH, Abakaliki BGH, Enugu Total overall

Parameter No. exam- Hb <11.0 g/dL No. exam- Hb <11.0 g/dL No. exam- Hb <11.0 g/dL
95% CI 95% CI 95% CI
ined No. % ined No. % ined No. %

Age (years)
HIV infection and anaemia in pregnancy

≤20 48 43 89.6 81.0-98.2 35 27 77.1 63.2-91.0 83 70 84.3 76.5-92.1

21-30 268 225 84.0 79.6-88.4 273 194 71.1 65.7-76.5 541 419 77.4 73.9-80.9

31-40 78 62 79.5 70.5-88.5 94 63 67.0 57.5-76.6 172 125 72.7 66.0-79.4

≥41 0 0 0.0 - 19 13 68.4 47.5-89.3 19 13 68.4 47.5-89.3

Total 394 330 83.8 80.2-87.4 421 297 70.5 66.1-74.9 815 627 76.9 74.0-79.8

Trimester

First 16 12 75.0 54.8-96.2 74 52 70.3 59.9-80.7 90 64 71.1 61.7-80.5

Second 138 124 89.9 84.9-94.9 178 137 77.0 70.8-83.2 316 261 82.6 78.4-86.8

Third 240 194 80.8 75.8-85.8 169 108 63.9 56.7-71.4 409 302 73.8 69.5-78.1

Total 394 330 83.8 80.2-87.4 421 297 70.5 66.1-74.9 815 627 76.9 74.0-79.8

HIV infection
90.6-
HIV positive 21 21 100.0 - 10 9 90.0 71.4-100.0 31 30 96.8
100.0
HIV negative 373 309 82.8 79.0-86.6 411 288 70.1 65.7-74.5 784 597 76.1 73.1-79.1

Total 394 330 83.8 80.2-87.4 421 297 70.5 66.1-74.9 815 627 76.9 74.0-79.8

BGH=Balm of Gilead Hospital, Enugu; CI=Confidence interval; EBSUTH=Ebonyi State University Teaching Hospital, Abakaliki; Hb=Haemoglobin
concentration
Uneke C.J et al.

JHPN
HIV infection and anaemia in pregnancy Uneke C.J et al.

anaemia at earlier stages of the disease (14). Iron Africa was described as usually most severe in the
deficiency has been described as the most common second trimester of gestation, especially following
cause of anaemia relating to nutrition (1). Other a period of acute infection, e.g. malaria, in the first
nutritional deficiencies (vitamin B12, folic acid, and trimester (11,13).
vitamin A), congenital blood disease, alpha-thala-
Our inability to assess other possible factors that
ssaemia, and glucose-6-phosphate deficiency)
may contribute to anaemia during pregnancy in
and some infections (hookworm, schistosomia-
the present study population was a major draw-
sis, or tuberculosis) may contribute to anaemia in
back to this investigation. The lack of any iron in-
pregnancy (3,4,6,7). Iron-deficiency anaemia has,
dicator, i.e. ferritin or serum transferrin receptor, is
however, assumed a major maternal health prob-
a major limitation of this study. Another limitation
lem in the subregion mainly because many people
of this study was the lack of information on the
cannot afford foods rich in haem iron, and other
disease stage of HIV-infected women. These limita-
dietary factors or cooking methods may inhibit
tions may have affected the adequate assessment
absorption of iron (6). This may have had a con-
of the contributory role of HIV infection on anae-
siderable contribution to anaemia observed in this mia observed among the subjects. Future research
study. Although it was reported that the dietary incorporating these aspects is advocated. This is
intake of iron by people living in developing coun- because despite multiple aetiologies of anaemia in
tries is generally high (36), iron deficiency remains pregnancy, they are all preventable. Therefore, the
prevalent in most developing countries, including knowledge of the relative importance of the differ-
Nigeria (37). This apparent paradox is because the ent causes of anaemia in pregnancy should form
iron being consumed is predominantly in the non- the basis for intervention strategies to control anae-
haem form, which is poorly absorbed, and some of mia (3).
this non-haem iron is from contamination of food
with iron from soil, dust, and water; iron leaching Since maternal and child-health services are the
into food during storage and cooking; contamina- most accessible health services in many commu-
tion during food processing, such as milling; and nities of the developing world, antenatal care ser-
the practice of geophagy (14,36). vices in particular could serve as the pivotal entry
point for simultaneous delivery of interventions
Furthermore, we observed from our study that most for the prevention and control of anaemia and HIV
pregnant women did not commence the intake of infection in pregnant women and their neonates
chemoprophylactic drugs, including haematinics with linkages to the community, child health, HIV
and folate, until they commenced to attend an- counselling and testing, treatment, care and sup-
tenatal care clinics. It was, therefore, not surprising port services, family planning, and other services
that the majority of the participants in this study (2,8,28,29). The transmission of HIV by blood
was anaemic as they were on their first visit to transfusion makes it more urgent to prevent anae-
antenatal care clinics since the commencement of mia and avoid the need for blood transfusions.
their present pregnancy and had not started tak- Therefore, public-health policies aimed at increas-
ing routine pregnancy drugs. Reports from vari- ing haemoglobin levels should continue to support
ous parts of sub-Saharan Africa have consistently programmes that provide iron supplementation.
indicated that women attending the antenatal care Screening and treatment for anaemia should be
clinic have a high prevalence of anaemia (6,7). The included in HIV care initiatives, particularly those
findings of this study, therefore, suggest that ante- that target women (14). The public-health signifi-
natal measures that can successfully target this cance of this cannot be overstated as the resolution
problem are of critical importance. Measures, such of HIV-related anaemia has been shown to improve
as routine chemoprophylaxis which is usually ad- the quality of life, physical functioning, energy,
ministered during visit to antenatal care clinic as and fatigue in individuals with HIV infection (38).
pregnancy progresses, have been found to be useful If coherence is ensured at each level of the mater-
in reducing anaemia (4). nal healthcare-delivery system in sub-Saharan
Africa, factors associated with anaemia which, of
When gestational age was related to anaemia, in- course, are largely preventable, and the effects of
terestingly, women in their second pregnancy anaemia on maternal health and pregnancy out-
trimester were significantly more anaemic than comes among HIV-infected and uninfected women
their counterparts in their first and third trimesters could be minimized with the use of cost-effective
(p<0.05). The reason for this outcome was not ap- and technologically-feasible public-health inter-
parently clear. However, anaemia in many areas of ventions.

Volume 25 | Number 3 | September 2007 333

HIV infection and anaemia in pregnancy Uneke C.J et al.

ACKNOWLEDGEMENTS 12. Axemo P, Liljestrand J, Bergstrom S, Gebre-Medhin

M. Aetiology of late fetal death in Maputo. Gynecol
The authors thank the Managements of Ebonyi Obstet Invest 1995;39:103-9.
State University Teaching Hospital, Abakaliki,
13. Brabin B, Piper C. Anaemia- and malaria-attributable
and Balm of Gilead Hospital, Enugu, for logistical
low birthweight in two populations in Papua New
support. The technical assistance offered by Mr. Guinea. Ann Hum Biol 1997;24:547-55.
Nwabueze Peter of the laboratory unit of Balm of
14. Antelman G, Msamanga GI, Spiegelman D, Urassa
Gilead Hospital, Enugu, is appreciated.
EJ, Narh R, Hunter DJ et al. Nutritional factors and
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