AIDS Behav (2009) 13:S66–S71
DOI 10.1007/s10461-009-9541-2
ORIGINALPAPER
Responding to Her Question: A Review of the Influence of
Pregnancy on HIV Disease Progression in the Context of
Expanded Access to HAART in Sub-Saharan Africa
Sarah MacCarthy Æ Fatima Laher Æ Mzikazi Nduna Æ
Lindiwe Farlane Æ Angela Kaida
Published online: 20 March 2009
Springer Science+Business Media, LLC 2009
Abstract In 2007, sub-Saharan Africa was home to over
half of all women living with HIV. The vast majority of
these women are of reproductive age, which raises con-
cerns about the high incidence of pregnancy. As access to
antiretroviral treatment is rapidly scaled up, two important
questions must be answered: (1) Does pregnancy impact
HIV disease progression?; (2) Does pregnancy modify the
highly active antiretroviral therapy (HAART) response on
HIV disease progression? A systematic review of the bio-
medical literature was conducted and seven relevant
studies were identified. To date, it appears that there is no
effect of pregnancy on HIV disease progression.
S. MacCarthy (&)
Department of Global Health and Population, Harvard School
of Public Health, 665 Huntington Avenue, Boston,
MA 02115, USA
e-mail: smaccarthy@hsph.harvard.edu;
smaccart@hsph.harvard.edu
F. Laher
Perinatal HIV Research Unit, Soweto, South Africa
M. Nduna
Department of Psychology, University of Witwatersrand,
Johannesburg, South Africa
L. Farlane
Engender Health, Johannesburg, South Africa
A. Kaida
BC Centre for Excellence in HIV/AIDS, Vancouver,
BC, Canada
A. Kaida
School of Population and Public Health, University of British
Columbia (UBC), Vancouver, BC, Canada
123
Furthermore, initial studies in high-income countries sug-
gest that pregnancy may positively modify the HAART
response. These findings, however, must be interpreted
with caution as it remains unclear how other factors, such
as adherence, may influence the relationship between
pregnancy, HIV disease progression, and HAART.
Keywords Pregnancy HIV Disease progression
HAART Sub-saharan Africa
Introduction
Sub-Saharan Africa (SSA) continues to be the world’s
most HIV/AIDS-affected region, with a reported 22.5
million adults and children living with the disease
(UNAIDS 2008). Contextualizing these figures within the
global pandemic illustrates the burden borne by SSA; more
than two out of three adults of the global HIV-positive
popu-lation live in the region. This trend does not appear to
be changing as over two-thirds of new infections globally
occur in SSA, and AIDS continues to be one of the leading
causes of death in the region (World Health Organization
2008).
Women in SSA are disproportionately affected by the
epidemic. In 2007, at 61%, SSA had the largest percentage
of women living with HIV. The vast majority of these
women are of reproductive age, which raises concerns
about the high incidence of pregnancy. Indeed a recent
review of pregnancy and HIV in SSA reported that 75% of
HIV positive women giving birth each year live in sub-
Saharan Africa (Gray and McIntyre 2007).
A 2008 progress report published by the World Health
Organization (WHO) highlights substantial global progress
in scaling-up access to services for the prevention of
AIDS Behav (2009) 13:S66–S71
mother-to-child transmission (PMTCT) of HIV. Between
2004 and 2007, the percentage of pregnant women living
with HIV with access to PMTCT in low and middle-
income countries increased from 10 to 33%. SSA has
shown the greatest rate of increased access to PMTCT over
the past 3 years, however, only 6% of pregnant women
receiving PMTCT in SSA are on highly active antiretro-
viral therapy (WHO 2008; WHO and UNAIDS 2008).
To date, most research exploring the effects of HAART in
pregnancy is narrowly focused on infant health (Eyakuze et al.
2008). Strategies to reduce the risk of vertical trans-mission,
such as mode of delivery and breastfeeding practices, are
recommended as effective ways to prevent perinatal infections
(The International Perinatal HIV Group 1999; WHO 2006).
The potential effects of HAART on pregnancy outcomes such
as low birth weight, premature birth and fetal death have also
received substantial attention (Suy et al. 2006; Szyld et al.
2006). While it remains important to understand how HAART
influences vertical transmission and pregnancy outcomes, it is
of equal impor-tance to understand the effect of HAART on
maternal health.
Some formative research on maternal outcomes associ-
ated with HAART use show an increased risk of pre-
eclampsia, gestational diabetes, toxicity and pregnancy-
induced hypertension (Conde-Agudelo et al. 2008; Kourtis
et al. 2006; Thorne and Newell 2007). Tuomala et al.
(2005) argued ‘‘the benefits of ART continue to outweigh
the risks’’ and underscored the importance of continued
research on the effects of HAART on maternal outcomes,
particularly as treatment regimens become increasingly
complex. Additional studies have produced contradictory
results, but the general consensus remains that the potential
side effects of HAART use for HIV-positive women
during pregnancy appear minimal, but further research is
required. As efforts move forward to understand the effect
of HA-ART on maternal outcomes, there remains a dearth
of research to determine the influence of pregnancy on
HIV disease progression.
Recent findings from qualitative research among HIV-
positive women in South Africa highlighted a great need to
synthesize current research concerning the relationship
between pregnancy and HIV disease progression in the
context of expanding access to HAART in SSA (Confer-
ence Summary Report 2008). As such, this systematic
review of the biomedical literature attempts to address two
important questions: (1) Does pregnancy impact HIV dis-
ease progression?; and (2) Does pregnancy modify the
HAART response on HIV disease progression? This
review is a critical step towards answering the questions
raised by the HIV-positive women by providing the
information necessary to achieve their reproductive goals
in a manner that maximizes maternal health.
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Methods
A systematic review of the literature was conducted to
identify studies examining the relationship between preg-
nancy and HIV disease progression in the context of
HAART. Pubmed and EMBASE databases were searched
because they both specialize in indexing the medical lit-
erature on the related topics of HIV, pregnancy and
HAART. A search strategy was designed in consultation
with a reference and education services librarian to ensure
that all relevant peer-reviewed articles were identified. In
each database, we used search terms relating to HIV
infections and/or AIDS; pregnancy, pregnancy complica-
tions or parturition; Antiretroviral Therapy, Highly Active
Antiretroviral Therapy (HAART); and HIV disease pro-
gression. Search strategies were limited to English
language articles published between January 1996 (the
year that HAART was introduced) and August 2008
(Gottlieb 2001).
Additionally, geographic limits were set to identify
studies from both sub-Saharan Africa and high-income
settings. The authors concluded that this distinction was
important to determine if other factors, such as income
level, influenced the relationship between the use of HA-
ART and pregnancy. The MeSH term ‘Africa South of the
Sahara’ was used to locate studies conducted in SSA. To
locate studies conducted in high-income settings, a search
strategy was designed to identify countries based on the
World Bank classification of countries based on income
(World Bank 2008).
The Pubmed search yielded 311 abstracts with poten-
tially relevant information. Two of the authors reviewed
the abstracts and identified five original research studies
that were specifically focused on pregnancy, HIV disease
progression, and HAART, and one systematic review, all
of which are included in this review. Similarly, the EM-
BASE search yielded 463 abstracts, from which one
additional included. To ensure that an appropriate satura-
tion of articles had been reached, we searched the citation
index, Web of Science, and reviewed the relevant refer-
ences cited in the seven articles included in our review. No
additional articles were identified.
For each of the six original research studies, we
reviewed the study design and study protocols including
recruitment strategies, durations of follow-up, outcome
assessments, participant retention, and associated limita-
tions. Three articles appropriately addressed the question:
‘‘Does pregnancy impact HIV disease progression?’’ and
the remaining three articles addressed the question: ‘‘Does
pregnancy modify HAART response on HIV disease
progression?’’ A review of these articles is presented
below.
123
S68
Results
Question 1: Does Pregnancy Impact HIV Disease
Progression?
A systematic review and meta-analysis examining the
effect of pregnancy on survival in women with HIV in
both low and high-income countries was published in 1998
(French and Brocklehurst 1998). To be included in this
review, studies had to have an appropriate control group
such that the effect of pregnancy in HIV-positive women
could be compared to a group of HIV-positive non-
pregnant women. Furthermore, studies were excluded if
they did not have the raw data available to conduct the
meta-analysis. Adverse outcomes assessed included
maternal death; maternal death attributable to HIV; HIV
progression (defined as progression from one CDC stage
of disease to another); the development of an AIDS
defining illness; and a fall in CD4 cell count to below 200
cells/mm3.
The review found that there does appear to be a rela-
tionship between adverse health outcomes and pregnancy
among HIV-positive women, however, the relationships
were not shown to be statistically significant. The reasons
for this finding were not elaborated on but were thought to
be a result of bias including residual confounding. They
did find, however, that HIV progression in pregnancy was
significantly more common in low-income country settings
than in high-income country settings.
Results from Sub-Saharan Africa
Subsequent to the review by French and Brocklehurst
(1998), a non randomized prospective cohort of 325 HIV-1
pregnant women in Abidjan, Cote d’Ivoire measured the
CD4 count and percentage at baseline (32 weeks of
amenorrhea) and at 1, 6 and 12 months after delivery.
Women received zidovudine (ZDV) beginning at 36 weeks
of gestation plus a single dose of nevirapine (NVP) during
labor for PMTCT. The variation noted in the absolute CD4
count between prepartum and postpartum periods was
attributed to the haemodilution effect of pregnancy. In
contrast, the CD4 percentage measurements remained sta-
ble suggesting that pregnancy has minimal impact on the
progression of HIV. The findings, though consistent with
the findings from the French and Brocklehurst review, are
limited by the lack of control group (Ekouevi et al. 2007).
Nonetheless, with the limited amount of information
available in SSA specifically on the relationship between
pregnancy and the progression of HIV, it is necessary to
review studies from high-income countries to adequately
answer the question.
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AIDS Behav (2009) 13:S66–S71
Results from High-Income Settings
A 17 center study in France enrolled 365 women with a
known date of HIV-1 seroconversion and compared the
progression to AIDS of pregnant women (n = 241) and non
pregnant women (n = 124). In addition, a sub-analysis
compared patients who had never conceived before
enrollment (n = 333) whether or not the date of serocon-
version was known. The women were examined every 3
months during pregnancy and every 6 months after
delivery until 2 years after delivery. Both analyses con-
firmed that pregnancy is not associated with the
progression of HIV disease. The authors noted potential
selection biases related to the fact that pregnancies not
carried to term were excluded, highlighting the possibility
that only healthier women carry pregnancies to term
(Saada et al. 2000).
From the European Study on the National History of
HIV Infection in Women and from the Swiss HIV cohort,
39 seropositive pregnant women were recruited. A review
of questionnaires and patient charts provided information
about the pregnancy, and CD4 lymphocyte counts were
obtained during pre-pregnancy, pregnancy and postpartum
visits. Different types of ARV regimens were available
over the course of follow-up, including no therapy,
monotherapy, dual therapy, and triple therapy. A
regression analysis determined that there was no statistical
difference between HIV-positive pregnant and non
pregnant women in terms of HIV disease progression. The
limitations of the study included the fact that only two
visits were scheduled in the European Women Study, the
date of conception was not known, and the information on
pregnancy was retro-spectively gathered and not confirmed
by laboratory markers (Van Benthem et al. 2002).
Consistent with findings from the Cote d’Ivoire study in
SSA, the two studies from high-income settings con-
cluded that pregnancy does not appear to negatively impact
HIV disease progression. These studies did not expressly
investigate whether pregnancy modifies the HAART
response on HIV disease progression. As we move into the
era of expanded access to HAART, we need to understand
whether pregnancy modifies the HAART response.
Question 2: Does Pregnancy Modify HAART
Response?
Sub-Saharan Africa
At the time of this review, there were no published studies
from SSA that examined whether pregnancy modifies the
HAART response on HIV disease progression.
AIDS Behav (2009) 13:S66–S71
High-Income Settings
In 2003, one of the first large scale prospective studies of
1,282 seropositive pregnant women in the US and Puerto
Rico assessed how HAART influences the progression of
HIV during pregnancy and postpartum (Minkoff et al.
2003). Four categories of treatment were established
between a single pregnancy group (n = 952) and a repeat
pregnancy group (n = 329), including no ART (n = 470),
monotherapy ZDV (n = 573), combination therapy (n =
120) and HAART (n = 179). Women were followed for at
least 12 months. The treatment categories were based on
clinician and patient discretion, rather than using stan-
dardized parameters across the study population. Maternal
CD4 percentage, viral load, adverse events and mortality
were assessed. The study concluded that of all regimens,
HAART raised the CD4 percentage the most (by 2% in 6
months). In addition, the authors found that women with a
second pregnancy had a lower risk of death and had no
significant effects on HIV disease progression. Two main
limitations relate to these findings: First, there were a small
number of women on HAART; Second, a selection bias
could influence the fact that only healthy women have
multiple pregnancies. The findings highlighted the need for
a more comprehensive understanding of the interaction
between the progression of HIV, pregnancy and HAART
(Minkoff et al. 2003).
A 2006 prospective multi-center study in London
explored the impact of HAART during pregnancy by
comparing women in three treatment arms: The cHAART
group consisted of women given HAART during preg-
nancy and continued post-partum (n = 155); The START
group consisted of women with a high viral load who
started HAART during pregnancy then discontinued use
after delivery (n = 71); and the ZDVm group received only
ZDV for PMTCT (n = 85). Women were assigned their
treatment category based their viral loads. The follow up
period was 33 months and the CD4, viral load, disease
progression, and incidence of MTCT were measured. With
access to HAART in pregnancy, Martin et al. (2006)
concluded that ‘‘progression to AIDS is infrequent.’’
However, there were two main limitations of this study:
First, 49 women were lost to follow up and second, there
were no matched cohort of HIV seropositive non pregnant
women (Martin et al. 2006).
An observational cohort study in the US recruited 759
seropositive women, of which 139 had more than one
pregnancy, from an outpatient clinic for HIV positive
women. Nearly three quarters (71%) of the study popula-
tion had received HAART, with no difference in HAART
duration by pregnancy status. Measuring CD4 count,
adverse events and mortality, a matched-pair analysis of
pregnant with non-pregnant seropositive women was
S69
conducted. The study reported that 8% of seropositive
pregnant women progressed to Class C event or death
compared with 24% of non-pregnant seropositive women.
After controlling for confounders, pregnancy was associ-
ated with a decreased risk of HIV disease progression. In
addition, the authors found that pregnancy was associated
with a decreased risk of disease progression both before
and after pregnancy. The authors noted that their findings
could be the result of the healthier immune status of
women who become pregnant or could possibly be related
to a beneficial interaction between pregnancy and
HAART. Limitations of the study include the fact that
there was minimal data on adherence, pregnant women
were fol-lowed up more frequently, and the authors were
unable to distinguish between AIDS related and non-AIDS
related deaths (Tai et al. 2007).
In summary, findings from Minkoff et al. (2003) indi-cate
that HIV-positive pregnant women on HAART have
improved maternal health and clinical outcomes (e.g., higher
CD4 percentage and lower viral load) compared with HIV-
positive pregnant women on all other treatment regimens,
including no treatment. Martin et al. (2006) reported that
HIV-positive women on HAART experienced similarly
positive changes in CD4, viral load, and HIV disease
progression compared with women on other anti-retroviral
regimens (i.e., START and ZDVm); however, there was no
control group of positive women who were not on treatment.
Together, these studies suggest that pregnant HIV-positive
women on HAART have the lowest risk of HIV disease
progression, compared with pregnant HIV-positive women on
other forms of treatment. More-over, none of the studies
reported a statistically significant increase in adverse maternal
health events in the HAART group compared with other
treatment regimens.
The Tai et al. (2007) study provides the strongest evi-
dence to date regarding the potential for pregnancy to
positively modify the HAART response. This study
showed that among HIV-positive women with access to
HAART, pregnancy is associated with a lower risk of HIV
disease progression or death. Indeed, pregnant women had
a lower risk of disease progression both before and after
the pregnancy event. It remains to be determined as to
whether these findings are generalizable to HIV-positive
women in SSA settings where access to HAART is
expanding rapidly.
Discussion
This systematic review of the literature focused primarily
on the biological mechanisms that may influence the way
pregnancy impacts the progression of HIV, first in the
absence of HAART, and then in the context of HAART. A
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S70
synthesis of these studies, both in SSA and high-income
countries, reinforces conclusions from earlier reviews that
pregnancy does not appear to influence the progression of
HIV. The present analysis also shows that in the context of
widespread access to HAART, pregnancy may positively
modify the HAART response. That is, among HIV-
positive women on HAART, those who become pregnant
are less likely to experience HIV disease progression,
suggesting a potential for a protective effect of pregnancy
among HIV-positive women on HAART.
The reasons for the potential protective effect of preg-
nancy in the context of access to HAART are unclear.
Three possible reasons proposed in a WHO and Joint
UNAIDS review of pregnancy and HIV include (WHO
and UNAIDS 1999):
1. The potential of an immunologic boost associated with
pregnancy.
2. A selection bias whereby women who are healthier
(and thus less likely to have HIV disease progression)
are more likely to become pregnant.
3. Adherence to HAART regimens during pregnancy
may improve due to increased concern about the well-
being of the fetus and/or due to increased contact with
the healthcare system for prenatal care.
These factors must be considered as HAART is
increasingly used during pregnancy. Furthermore, as
women on more complex regimens become pregnant, the
effects of HAART on maternal health must continually be
reassessed.
Particularly for SSA, the protective effect of pregnancy
must be interpreted with caution as other structural factors
may influence the relationship between pregnancy and
HAART (Mellins et al. 2008). Adherence to HAART by
HIV positive women can be influenced by both access and
HIV-related stigma. Focusing first on access, we see that
discrepancies in access, both between countries and within
countries, continue in SSA (World Health Organization
2008). The organization of the clinics alone raises a series
of considerations for pregnant women with HIV: How long
does it take to get to the clinic? Who will care for the
family in her absence? Once at the clinic, how long must
she wait to receive care? If she is able to access treatment,
adherence continues to be complicated by the woman’s
ability to take care of her own health, dealing with
potential side affects from toxicity, in addition to other
responsi-bilities as the primary caregiver. Questions
surrounding access will continue to persist as a priority
issue as HA-ART is scaled up in SSA.
Another factor that may influence adherence to HAART
is HIV-related stigma experienced by women both during
and after pregnancy. Even if treatment is accessible, the
fear of HIV-related stigma may inhibit women from
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AIDS Behav (2009) 13:S66–S71
seeking treatment. Disclosing HIV status may have
implications on the individual, community, and national
levels. On the individual level, recent studies have shown
that disclosure of HIV positive status can result in
increased violence experienced by women (Jansen van
Rensburg 2007). On the community level, studies show
that HIV positive women experience isolation from their
communities once their status is discovered (Dlamini et al.
2007). And on the national level, HIV can be criminalized
through punitive laws that further enforce the stigmatiza-
tion of people living with HIV (Burris and Cameron 2008).
Consequently, as increased funding may lead to even
greater availability of treatment, the potential barriers to
treatment must be considered at all levels.
Access and HIV-related stigma are only two examples
of the way in which the relationship between HIV, preg-
nancy and HAART may be mediated by adherence. Initial
studies on adherence during pregnancy show conflicting
results (Karchar et al. 2007; Zorrilla et al. 2003), high-
lighting the need to research how behavior, not just
biology, may affect the way in which pregnancy impacts
the progression of HIV, both in the absence and presence,
of HAART.
Conclusion
A review of the current literature suggests that there is no
effect of pregnancy on HIV disease progression. Further-
more, initial studies in high-income countries suggest that
pregnancy may positively modify the HAART response,
however, it remains to be determined whether or not the
relationship is a result of HAART or other potential
factors. While these recent findings are important for the
clinicians providing care to HIV-positive women of
reproductive age, they may have even greater relevance to
HIV positive-women who have been waiting for a
response to their questions.
Acknowledgments The authors are thankful to Carol Mita for her
assistance in the design and review of the search strategy used in this
article.
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