OBSTETRICS
A Ten-Year Review of Antenatal Complications
and Pregnancy Outcomes Among HIV-Positive
Pregnant Women
Mark H. Yudin, MD, MSc,1 Daniela Caprara, MD, MSc,1 S. Jay MacGillivray, RM,1
Marcelo Urquia, PhD,2 Rajiv R. Shah, MD, MSc1
1
Department of Obstetrics and Gynecology, St. Michael’s Hospital, University of Toronto, Toronto, ON
2
Keenan Research Centre, Li Ka Shing Knowledge Institute, University of Toronto, Toronto, ON
Abstract
Objective: To review the incidence of antenatal complications among a
cohort of HIV-positive pregnant women over a 10-year period.
Methods: A retrospective review was performed of all HIV-positive
pregnant women receiving multidisciplinary prenatal care at an
urban tertiary care centre from March 2000 to March 2010.
Collected data included the presence of additional infectious or
medical conditions, genetic screening information, and the
presence or absence of antenatal complications.
Results: One hundred and forty-two singleton pregnancies during the
study period were identified. Almost 95% of women were taking
combination antiretroviral therapy during pregnancy, and greater
than 90% had viral loads less than 1000 copies/ml at delivery. The
presence of co-infections was low. Forty-one women (29%) had
other medical comorbidities. Genetic screening occurred in 104
pregnancies (73%); 4% were abnormal screens. Rates of any
hypertension, gestational diabetes, and fetal growth restriction were
all low. Thirty-two percent of women were colonized with group B
streptococcus.
Conclusion: This study adds strength to the argument that good
outcomes can be achieved for HIV-positive pregnant women with
good access to both prenatal and HIV care, and appropriate
management. Women with HIV should be optimally cared for in
Key Words: HIV, pregnancy, pregnancy complications, pregnancy
outcomes
This work was presented in part or in whole at:
 The Annual Meeting of the Society of Obstetricians and Gynaecol-
ogists of Canada (SOGC), June 24, 2011, Vancouver, British Columbia,
Canada
 The Annual Meeting of the Canadian Conference on HIV/AIDS
Research, April 20, 2012, Montreal, Quebec, Canada
 The Annual Meeting of the Society of Obstetricians and Gynaecol-
ogists of Canada (SOGC), June 11, 2015
Competing Interests: None declared.
Received on April 2, 2015
Accepted on July 24, 2015
http://dx.doi.org/10.1016/j.jogc.2015.10.013
advance of and during pregnancy in order to maximize the
likelihood of good pregnancy outcomes.
Résumé
Objectif : Analyser l’incidence, sur une période de 10 ans, des
complications prénatales chez une cohorte de femmes enceintes
séropositives pour le VIH.
Méthodes : Nous avons mené une analyse rétrospective portant sur
toutes les femmes enceintes séropositives pour le VIH qui ont reçu
des soins prénataux multidisciplinaires au sein d’un centre urbain
de soins tertiaires entre mars 2000 et mars 2010. Parmi les
données recueillies, on trouvait la présence de troubles infectieux
ou médicaux additionnels, les résultats du dépistage génétique et
la présence ou l’absence de complications prénatales.
Résultats : Au cours de la période d’étude, nous avons identifié
142 grossesses monofœtales. Pratiquement 95 % des femmes
avaient reçu un traitement par association d’antirétroviraux pendant
la grossesse et plus de 90 % d’entre elles présentaient des charges
virales inférieures à 1 000 copies/ml au moment de l’accouchement.
La présence de co-infections était faible. Quarante et une femme
(29 %) présentaient d’autres comorbidités médicales. Un dépistage
génétique avait été mené dans le cadre de 104 grossesses (73 %);
4 % d’entre elles ont obtenu des résultats anormaux. Les taux
d’hypertension (quelle qu’elle soit), de diabète gestationnel et de
retard de croissance intra-utérin étaient tous faibles. Une
colonisation par des streptocoques du groupe B a été constatée
chez 32 % de ces femmes.
Conclusion : Cette étude soutient l’hypothèse selon laquelle il est
possible pour les femmes enceintes séropositives pour le VIH
d’obtenir de bonnes issues lorsqu’elles disposent d’un bon accès à
des soins prénataux et contre le VIH, et à des services de prise en
charge adéquats. Pour maximiser la probabilité d’obtenir de bonnes
issues de grossesse, les femmes enceintes séropositives pour le
VIH devraient faire l’objet de soins optimaux avant et pendant la
grossesse.
Copyright ª 2016 The Society of Obstetricians and Gynaecologists of
Canada/La Société des obstétriciens et gynécologues du Canada.
Published by Elsevier Inc. All rights reserved.
J Obstet Gynaecol Can 2016;38(1):35e40
JANUARY JOGC JANVIER 2016 l 35
OBSTETRICS
INTRODUCTION
T here are more than 71 000 HIV-positive individuals
currently living in Canada, and over the past decade
the proportion of these who are female has remained
stable at approximately one quarter of all cases.1 At least
75% of Canadian HIV-positive women are of child-bearing
age, and HIV infection is diagnosed in Canadian women at
a younger age than in Canadian men.2 Individuals who are
currently HIV-positive are likely to live a healthy and
productive life, leading to increasing numbers of preg-
nancies among HIV-positive women in developed coun-
tries such as Canada.3,4
There is an emerging body of literature reporting on
maternal and perinatal outcomes among HIV-positive
women. Much of this information is conflicting, with
some studies reporting increased rates of adverse out-
comes (such as preterm birth, growth restriction, pre-
eclampsia and gestational diabetes) and others reporting no
increase in this risk, compared to HIV-negative wom-
en.5e19 Further, these studies have been conducted in a
variety of geographic locations and with heterogeneous
populations, varying degrees of medication adherence and
immune function. These factors and others have been
suggested as confounders which may affect the associa-
tions between HIV-positivity and adverse outcomes.
We recently reported on a cohort of HIV-positive pregnant
women cared for in Toronto, Ontario over a 10-year
period.3 The majority of these women had prenatal care
throughout their pregnancy and had well-controlled HIV
infection, with 94% being treated with combination anti-
retroviral therapy (cART) and more than 90% having viral
loads less than 1000 copies/mL at the time of delivery.
The primary objective of this study was to report the
antenatal complications and pregnancy outcomes of this
cohort of well-controlled HIV-positive women having
multidisciplinary prenatal care in one major Canadian
centre.
METHODS
This study was a retrospective chart review of all HIV-
positive pregnant women cared for at St. Michael’s Hos-
pital in Toronto, Ontario from March 2000 to March
2010. Cases were identified using an internal hospital ob-
stetric database and using chart codes with the aid of
hospital decision support. In this way, we were able to
perform two independent searches to confidently identify
all eligible women during the study period. The final
cohort included all singleton pregnancies; first trimester
36 l JANUARY JOGC JANVIER 2016
losses were excluded. All charts were reviewed by a single
reviewer (D.C.) and data were collected using a standard-
ized data sheet and transferred to a Microsoft Excel
(Microsoft Corp., Redmond, WA) file. Both electronic and
paper charts were used for data collection and all data were
anonymized before analysis. Data collected have been
previously described,3 but, for the present analysis, rele-
vant data included the presence of additional infections or
medical conditions, genetic screening information, and the
presence or absence of antenatal and intrapartum com-
plications such as preterm birth (defined as birth < 37
weeks’ gestation), gestational diabetes (diagnosed by hav-
ing an abnormal result from a 2-hour glucose tolerance
test), hypertension (diagnosed as blood pressure greater
than 140/90 or requiring antihypertensive medication with
pre-existing/chronic hypertension either predating preg-
nancy or occurring up to 20 weeks gestation, and gesta-
tional hypertension occurring at 20 weeks gestation or
greater), preeclampsia (defined as pre-existing/chronic or
gestational hypertension combined with new or worsening
proteinuria or one/more adverse conditions or one/more
severe complications), fetal growth abnormalities (defined
as growth less than the 10th percentile growth for gesta-
tional age by ultrasound assessment), abnormal ultrasound
findings, and group B streptococcus (GBS) status.
The distribution of study variables was examined using
frequencies, with categorical variables expressed as counts
and percentages, and continuous or discrete variables
expressed as means and ranges. Bivariate analyses included
cross-tabulations. Associations between categorical vari-
ables were assessed with the chi-square test. Assessment of
trends was performed using the Cochrane-Armitage test
for binomial proportions. A P-value < 0.05 was used as
the cutoff for statistical significance. All statistical tests
were conducted using SAS 9.3 (SAS Institute Inc., Cary,
NC).
Approval for the study was obtained from the St Michael’s
Hospital Research Ethics Board.
RESULTS
Between March 2000 and March 2010, 142 singleton
pregnancies in HIV-positive women were identified at our
institution. Two sets of twins and one early pregnancy loss
were excluded. Almost 94% (133/142) of women were on
cART during pregnancy. Of 128 with recorded viral loads
at delivery, 98 (77%) were undetectable and 118 (92%)
were 1000 copies/mL or less. The presence of co-
infections among our cohort is presented in Table 1.
 A Ten-Year Review of Antenatal Complications and Pregnancy Outcomes Among HIV-Positive Pregnant Women
Table 1. Presence of Co-Infections Among HIV-Positive
Pregnant Women
Infection n (%)
Syphilis 4 (3%)
Hepatitis B 8 (6%)
Hepatitis C 2 (1%)
Gonorrhea/Chlamydia 3 (2%)
Rubella non-immune 12 (8%)
Forty-one women (29%) had comorbidities, the most
common being tuberculosis, asthma, and hypertension
(Table 2). Alcohol and drug use was low in this cohort,
with 80% (113/142) non-smokers; only three women (2%)
admitted to alcohol use and five (4%) admitted to illicit
drug use.
Genetic screening by maternal serology was commonly
performed in this cohort of women, with 104 (73%)
completing testing and 4 (4%) had an abnormal result. One
of these women chose to undergo amniocentesis after
being given an estimated risk of trisomy 21 of 1:4. She was
on cART and had an undetectable viral load at the time of
amniocentesis. Amniocentesis revealed a normal karyotype.
No genetic abnormalities occurred in the entire cohort,
including among the women with abnormal serologic
screens. The most common reason for not being tested
was presenting to care too late.
The mean gestational age at delivery was 38.1 weeks. The
preterm birth rate was 19%, with no difference found in the
rates of preterm birth between women on protease inhibitor
(PI)-containing regimens compared to those without PIs (P
> 0.05); 65% were late preterm births (more than 34 weeks’
gestational age), and only six births were less than 30 weeks.
Of the total 27 preterm births, 17 resulted from sponta-
neous preterm labour, and 10 were induced. The most
common reason for preterm induction of labour was pre-
term premature rupture of membranes (7/10). There was
one induction for growth restriction at 36 weeks gestation,
one for preeclampsia at 34 weeks gestation, and one for
intrauterine fetal death at 25 weeks gestation.
The incidence of gestational diabetes and any hypertension
was low in this cohort of women. Nine women (6%) had
gestational diabetes; five of these were controlled with
diet alone and four required insulin. All of those with diet
control were on a PI (lopinavir/ritonavir or nelfinavir) and
only one requiring insulin was on a PI (nelfinavir). Seven
women (5%) had hypertension as a complication in preg-
nancy; one had pre-existing hypertension and the
remainder had gestational hypertension. Only one woman
Table 2. Medical Comorbidities Among HIV-Positive
Pregnant Women
Medical Comorbidity n (%)
Tuberculosis 10 (7%)
Asthma 6 (4%)
Hypertension 6 (4%)
Malaria 3 (2%)
Anemia 2 (1%)
Pyelonephritis 2 (1%)
Other 12 (8%)
required pharmacologic treatment. Two of these women
developed preeclampsia requiring induction of labour, one
at 34 and the other at 38 weeks gestation.
The incidence of ultrasound abnormalities was low, with
fetal anatomic anomalies infrequently observed. There
were four fetuses (3%) with echogenic intracardiac foci,
three (2%) with pelviectasis, and one with a choroid plexus
cyst. Three pregnancies (2%) had abnormal Doppler flow
studies, and five (4%) had intrauterine growth restriction.
Four of these had growth between the third and tenth
percentile, and one case was below the third percentile. All
of these women were on PIs (either lopinavir/ritonavir,
nelfinavir, or atazanavir).
In the entire cohort, 45 women (32%) were positive for
GBS.
Mode of delivery was vaginal in 87 (61%) and Caesarean
section in 55 (39%) women. In our program, HIV-exposed
infants are followed for five years after birth. HIV poly-
merase chain reaction (PCR) testing is performed at birth,
one month, and two months of age. HIV serology is
performed at 18 months of age to confirm clearance of
maternal antibody. All infants remained HIV-negative.
DISCUSSION
In this 10-year cohort of 142 pregnancies in well-controlled
HIV-positive women, we found low rates of co-infection
and serious comorbidities, abnormal genetic screening
tests, and pregnancy complications. Positive GBS culture
rates were higher than among the general population at the
study institution.
Studies addressing outcomes in pregnancies complicated by
HIV have reported conflicting information, with some
demonstrating higher risks for adverse outcomes, and others
showing no difference in these risks between HIV-positive
and HIV-negative women.10e19 Further, some antiretroviral
drugs have been implicated more than others. These studies
JANUARY JOGC JANVIER 2016 l 37
OBSTETRICS
have been conducted in diverse global locations and with
heterogeneous populations of HIV-positive women, with
varying degrees of medication adherence and immune
function. These factors and others, such as ethnicity, smok-
ing, and alcohol and drug use, may be confounders and affect
the degree of strength of the associations found between HIV
status and adverse outcomes in pregnancy. Understanding
these risks from these various studies is challenging.
Most of the initial work demonstrating an increase in the risk
of preterm birth among women on cART originated in
Europe, with preterm delivery rates up to three times higher
in women taking these medications.10e13 Some of these
studies, as well as studies from Africa, implicated PIs as the
drugs associated with the highest risks.14 Subsequent studies
from North America did not show an increase in preterm
birth risk among women on cART.15e17 A meta-analysis of
studies published up until 2006 reported no association be-
tween cART and increased risk of preterm delivery overall
(OR 1.01; 95% CI 0.8 to 1.3), although there was an
increased risk seen among women on PI-containing regimens
(OR 1.35; 95% CI 1.1 to 1.7).18 More recent work from
France has also demonstrated an increase in the preterm
birth rate among women on cART (OR 1.69; 95% CI 1.38 to
2.07), and particularly in women taking ritonavir-boosted PI
therapy (adjusted hazard ratio 2.03; 95% CI 1.06 to 3.89).19
In our cohort, the preterm birth rate was 19%, higher than
the national average; of approximately 8%.20 an increased
risk for preterm delivery among women on PI-containing
regimens was not demonstrated in the current study. The
current study was not statistically powered to detect a dif-
ference in the risk for preterm birth, an outcome with a
recognized multifactorial etiology. We are currently con-
ducting a prospective study of matched cohorts of HIV-
positive and HIV-negative women to better understand the
preterm birth rates and risks in the HIV-positive population.
The rates of both gestational diabetes and any hypertension
were low in our cohort (5% each. The effect of antire-
troviral drugs on glucose metabolism and insulin resistance
among pregnant women remains poorly understood, and
there have been conflicting results in the literature with
respect to the risk of gestational diabetes in HIV-positive
women.7,21,22 Gestational diabetes complicates 2% to 5%
of pregnancies among women in North America,23 and the
rate in our cohort (6%) was similar. Gonzalez-Tome et al.
specifically implicated PIs as a risk for developing gesta-
tional diabetes,7 but others have concluded that PIs do not
increase the risk.21,22 Six of the nine women who devel-
oped gestational diabetes in this cohort were on PI-
containing drug regimens. The association between
cART and gestational diabetes remains unclear.
38 l JANUARY JOGC JANVIER 2016
Observational and cohort studies evaluating the risk for
hypertension disorders in pregnancies complicated by HIV
have suggested that the risk is increased,8 while matched
cohort studies from Canada and the United States have not
demonstrated this increase.9,24 In the current study, six
women developed hypertension during pregnancy; two of
these developed preeclampsia.
Most women who were eligible for serologic genetic
screening (and who presented for care early enough in
pregnancy) accepted testing, and four women had positive
screens. Multiple marker serum testing has been shown to be
reliable in HIV-positive pregnant women with no difference
in the likelihood of false positive tests, although multiples of
the median levels of specific hormone markers may differ
between HIV-positive and negative women.25,26 Genetic
screening is an important issue for pregnant women, but the
option of reliable serologic screening is important for HIV-
positive women, as it may help to avoid the need for inva-
sive testing such as amniocentesis or chorionic villus sam-
pling. Lopez and Coll have suggested that the risk of HIV
transmission due to invasive procedures such as amnio-
centesis is low, since they had no cases of transmission
among 159 women on cART.27 National guidelines now
state that amniocentesis performed in women on cART does
not appear to increase the risk of transmission, especially if
the viral load is undetectable, but that women should be
counselled that data are limited. Prenatal risk assessment is
recommended, using tests with high sensitivity and low false-
positive rates, such as serum screening combined (or not)
with nuchal translucency, anatomic ultrasound, and non-
invasive molecular prenatal testing.28
There was a low incidence of fetal ultrasonographic ab-
normalities in our cohort, and no serious fetal anomalies
occurred. Antiretroviral drugs are not believed to be tera-
togenic; a recent meta-analysis of 21 studies showing no
difference in the likelihood of birth defects between infants
born to mothers on efavirenz-based and nonefavirenz-
based regimens.29 Fetal growth restriction was also rare in
the current study. The risk of fetal growth abnormalities has
not been consistently reported, with some studies reporting
an increased risk and others showing no increase in risk,30
and no association was observed in studies accounting for
confounding variables. In a Canadian matched cohort study,
there was no difference in the risk of growth restriction
between HIV-positive women and an HIV-negative
matched control group.9 In an American prospective
observational study, HIV severity was associated with an
increased risk of fetal growth abnormalities after adjusting
for sociodemographic variables, medication use and disease
severity; cART use was not associated.31
 A Ten-Year Review of Antenatal Complications and Pregnancy Outcomes Among HIV-Positive Pregnant Women
The rate of GBS positivity in this cohort was 32%, which is
higher than the baseline population rate of 22% at our insti-
tution.32 In one study of 90 HIV-positive pregnant women,
HIV status was not independently associated with GBS colo-
nization,33 although the overall relationship remains unclear.
Adverse maternal and perinatal outcomes may be associ-
ated with HIV-positivity, combination or specific antire-
troviral drug use, or the presence of confounding factors.
It has previously been hypothesized that one of the most
important confounding variables in the association be-
tween adverse outcomes and HIV-positivity is disease
severity.13,17,31 In the current study, most women had well-
controlled HIV infection, adequate prenatal care, and low
rates of substance use and co-morbidities; rates of ante-
natal complications were low, and pregnancy outcomes
were favourable.
Many studies to date have evaluated outcomes in HIV-
positive women with poor access to care and with poorly
controlled disease, and outcomes may differ between these
populations. Retrospective studies are limited by their reli-
ance on data extracted from chart review. The cohort in the
present study was from a single centre and may not be fully
representative of a more diverse population. Finally, there
was no control group with which to compare outcomes.
CONCLUSION
This important study evaluated pregnancy outcomes in HIV-
positive women and demonstrated favourable outcomes in
women with appropriate access to multidisciplinary prenatal
and HIV care and with well-controlled disease. The study
adds strength to the argument that good outcomes can be
achieved for HIV-positive pregnant women with appropriate
management and good access to both prenatal and HIV care.
HIV-positive women should be optimally cared for in
advance of and during pregnancy in order to maximize the
likelihood of good pregnancy outcomes.
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