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Original Research

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OBSTETRICS

Trends in hospitalizations of pregnant HIV-infected


women in the United States: 2004 through 2011
Alexander C. Ewing, MPH; Hema M. Datwani, MD; Lisa M. Flowers, MPA;
Sascha R. Ellington, MSPH; Denise J. Jamieson, MD; Athena P. Kourtis, MD

BACKGROUND: With the development and widespread use of combination antiretroviral therapy, HIV-infected women live longer, healthier
lives. Previous research has shown that, since the adoption of combination
antiretroviral therapy in the United States, rates of morbidity and adverse
obstetric outcomes remained higher for HIV-infected pregnant women
compared with HIV-uninfected pregnant women. Monitoring trends in the
outcomes these women experience is essential, as recommendations for
this special population continue to evolve with the progress of HIV treatment and prevention options.
OBJECTIVE: We conducted an analysis comparing rates of hospitalizations and associated outcomes among HIV-infected and HIV-uninfected
pregnant women in the United States from 2004 through 2011.
STUDY DESIGN: We used cross-sectional hospital discharge data
for girls and women age 15e49 from the 2004, 2007, and 2011
Nationwide Inpatient Sample, a nationally representative sample of US
hospital discharges. Demographic characteristics, morbidity outcomes,
and time trends were compared using c2 tests and multivariate logistic
regression. Analyses were weighted to produce national estimates.
RESULTS: In 2011, there were 4751 estimated pregnancy hospitalizations and 3855 delivery hospitalizations for HIV-infected pregnant
women; neither increased since 2004. Compared with those of

Introduction
Recommendations for HIV screening of
pregnant women and treatment of
pregnant women with HIV infection
have led to a dramatic decrease in the
rate of mother-to-child transmission of
HIV to <2% in the United States.1-4
Recent US guidelines recommend combination antiretroviral (ARV) therapy
(cART) as the standard of care for all
HIV-infected individuals, and such
therapy is particularly critical for
pregnant women.3,5 With the development and widespread use of cART,
HIV-infected women are living longer,
healthier lives.6-8 From 2000 through

Cite this article as: Ewing AC, Datwani HM, Flowers LM,
et al. Trends in hospitalizations of pregnant HIV-infected
women in the United States: 2004 through 2011. Am J
Obstet Gynecol 2016;volume:x.ex-x.ex.
0002-9378/$36.00
Published by Elsevier Inc.
http://dx.doi.org/10.1016/j.ajog.2016.05.048

HIV-uninfected women, pregnancy hospitalizations of HIV-infected women


were more likely to be longer, be in the South and Northeast, be covered by
public insurance, and incur higher charges (all P < .005). Hospitalizations
among pregnant women with HIV infection had higher rates for many
adverse outcomes. Compared to 2004, hospitalizations of HIV-infected
pregnant women in 2011 had higher odds of gestational diabetes
(adjusted odds ratio, 1.81; 95% confidence interval, 1.16e2.84), preeclampsia/hypertensive disorders of pregnancy (adjusted odds ratio, 1.58;
95% confidence interval, 1.12e2.24), viral/mycotic/parasitic infections
(adjusted odds ratio, 1.90; 95% confidence interval, 1.69e2.14), and
bacterial infections (adjusted odds ratio, 2.54; 95% confidence interval,
1.53e4.20). Bacterial infections did not increase among hospitalizations
of HIV-uninfected pregnant women.
CONCLUSION: The numbers of hospitalizations during pregnancy and
delivery have not increased for HIV-infected women since 2004, a departure from previously estimated trends. Pregnancy hospitalizations of
HIV-infected women remain more medically complex than those of HIVuninfected women. An increasing trend in infections among the delivery
hospitalizations of HIV-infected pregnant women warrant further attention.
Key words: delivery, HIV, hospitalization, pregnancy, United States

2006, estimated rates of childbearing


increased among HIV-infected women
and more such women desired
pregnancy.6,9
Despite the benets of cART for the
treatment and prevention of HIV, there
are concerns about potential adverse effects to the pregnant woman, fetus, and
newborn. ARV drugs have been linked
with hyperglycemia, diabetes mellitus,
lactic acidosis, hepatic steatosis, and
renal and hepatic toxicity,5,10-15 although
studies of their effects in pregnancy have
generated conicting results.16,17 Some
studies have shown an increased risk
for preeclampsia among HIV-infected
women receiving ARV drugs compared
to HIV-uninfected women, but these
ndings have been inconsistent.18-20 In
addition, there are conicting ndings
on ARV drugs and risk of preterm
delivery.21-30 Many of these studies of
pregnancy outcomes among women
with HIV infection are limited by relatively small sample size, retrospective

design, and no adjustment for possible


confounding factors.
In a previous nationwide analysis
of trends of hospitalizations among
HIV-infected pregnant women in the
United States from 1994 through
2003, we described higher rates of
morbidity and adverse obstetric outcomes among HIV-infected, compared
with
HIV-uninfected,
pregnant
women.31 Of note, during that time,
there was no increase in the rate of preterm labor, preterm delivery, or preeclampsia/hypertension (HTN) among
pregnant HIV-infected women in the
United States.31 Since this analysis was
published, additional ARVs have
become available, recommended rstline cART regimens during pregnancy
have changed, and most HIV-infected
women who know their status now
receive cART prenatally and during labor
and delivery. Given these changes, the
objectives of our analysis were to use
more recent data from the Healthcare

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Original Research

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Cost and Utilization Project (HCUP),


obtained during a period of widespread
cART availability, to examine trends of
adverse outcomes that could be related
to HIV infection or its treatments among
pregnant women in the United States.
Monitoring these trends is essential, as
recommendations for this special population continue to evolve with the
progress of HIV treatment and prevention options.

Materials and Methods


We obtained US hospital discharge data
from the HCUP Nationwide Inpatient
Sample (NIS). HCUP is a family of
health care databases and related software tools sponsored by the Agency for
Healthcare Research and Quality in
partnership with state-level data
collection organizations.32 The NIS is a
20%-stratied probability sample of US
community hospitals dened by the
American Hospital Association as
nonfederal, short-term (average length
of stay <30 days) general and specialty
hospitals with facilities open to the
public. Hospitals were sampled based on
5 strata: rural/urban location, number of
beds, region, teaching status, and
ownership. In each year spanning 2004
through 2011, NIS included inpatient
stays from about 1000 hospitals with 7-8
million discharge records annually that
were weighted to enable production of
national estimates.33 The NIS is one of
the largest collections of all-payer inpatient data and includes hospital charge
and length-of-stay data. Discharge data
include International Classication of
Diseases, Ninth Revision, Clinical Modication (ICD-9-CM) diagnosis and
procedure codes, as well as DiagnosisRelated Groups and Clinical Classication Software (CCS) diagnostic codes for
ICD-9-CM, a uniform and standardized
diagnosis and procedure categorization
scheme.34
We analyzed NIS data from 2004
through 2011, a period in which the
number of states included in the NIS
increased from 37-46.34,35 Our analysis
was restricted to antenatal and delivery
pregnancy hospitalizations. The women
referred to in this study include girls
and women 15e49 years of age. We

identied hospitalizations of pregnant


women (ICD-9-CM codes 640-677,
V22-V24, V27-V28, 792.3), and then
identied those resulting in delivery
(ICD-9-CM codes 650, V27; ICD-9-CM
procedure codes 72.0-72.9, 73.22,
73.59, 73.6, 74.0-74.2, 74.4, 74.99; and
Diagnosis-Related Group codes 370375). We excluded those for ectopic/
molar pregnancy or spontaneous abortion (ICD-9-CM codes 630, 631, 633,
632, 634-639; procedure codes 69.01,
69.51, 74.91, 75.0).
The ICD-9-CM codes used in this
analysis to identify hospitalizations
complicated by preterm labor or rupture
of membranes, preterm delivery, gestational diabetes mellitus (GDM), preeclampsia/HTN disorders of pregnancy,
antepartum hemorrhage, major puerperal infection, and HIV have been
described previously.31 The denitions of
certain morbidities and outcomes used in
the previous analysis were modied as
follows: (1) liver disorders of pregnancy,
including hepatic steatosis, lactic
acidosis, and elevated liver function tests
(276.2, 571.8, 646.7, 790.4, 573.3, 573.9);
(2) sexually transmitted infections and
pelvic inammatory disease (647.0647.2, 090.0-099.9, 054.5, 054.7, 079.88,
614.0-614.5, 614.7-614.9, 615, 616);
(3) bacterial infections (CCS codes 2, 3);
(4) viral, mycoses, parasitic, and other
infections (CCS codes 4, 6, 7, 8, 77,
78, 126); (5) inuenza and pulmonary
complications (480-488); and (6) urinary
tract infections (646.6, 590, 595, 597,
599.0). Finally, we included the following
conditions for use as adjustment variables: anemia (648.2, 280-285), hepatitis
B and C (070.2-070.3, 070.41, 070.42,
070.44, 070.51, 070.52, 070.54, 070.7),
drug use (304, 305.2-305.9), alcohol
abuse (303.0, 303.9, 305.0, 291.0, 291.4,
291.81), and smoking (305.1, 649.0).
We used Student t test and the Wald c2
test with a signicance level of .05 to
compare demographic and hospital
characteristics and outcomes, as well as
length of hospitalization and hospital
charges, of hospitalized HIV-infected vs
HIV-uninfected pregnant women. We
compared the following patient or
hospital characteristics: age distribution, expected primary payer, median

household income quartile based on


patient ZIP code, urban/rural hospital,
geographic region of the hospital, total
and mean length of hospital stay, total
and mean hospital charges for hospitalization, and inpatient mortality rate. All
hospital charge data are adjusted for
ination and presented in 2011 dollars.
For 2004 through 2011, we compared
odds of adverse outcomes among
hospitalizations of HIV-infected, vs
HIV-uninfected, women using multivariable logistic regression, adjusting for
demographic variables and relevant
comorbidities. To assess the trend in
absolute number of delivery hospitalizations for HIV-infected women per
year in the study period, we used a
weighted least squares regression
designed specically for use with survey
data.36 To assess trends in outcomes, we
compared data from 2007 through 2011
with that from 2004 (reference year),
adjusting for maternal age, expected
payer, and delivery status in logistic or
linear regression models, according to
outcome type. Models with interaction
terms were run to assess whether the
magnitude of changes over time differed
according to HIV status. Subanalyses
were conducted to examine whether
the associations between HIV and
outcomeseincluding hospital charges,
length of stay, and bacterial infectione
were modied by hospitalization type
(delivery or antenatal). All statistical
analyses were conducted with survey
procedures using software (SAS, Version
9.3; SAS Institute, Cary, NC). As a secondary analysis of a deidentied data set,
this study was exempt from institutional
review board approval.

Results
The number of hospitalizations and deliveries among HIV-infected pregnant
women did not increase over the study
period (trend test P value: .569). There
were an estimated 7107 hospitalizations
of pregnant HIV-infected women in
2004, 6837 in 2007, and 4751 in 2011.
The 2011 estimate is 33% lower than in
2004; in comparison, the corresponding
estimate for HIV-uninfected women was
11% lower in 2011 than in 2004.
There were an estimated 5339 delivery

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hospitalizations for pregnant HIVinfected women in 2004, 5397 in 2007,


and 3855 in 2011. The 2011 estimate is
28% lower than in 2004; the corresponding estimate for HIV-uninfected
women was 9% lower in 2011 than
in 2004.
From 2004 through 2011, hospitalizations of HIV-infected pregnant women
represented an estimated 0.11-0.15% of
all hospitalizations of pregnant women
in the United States. The number of

Original Research

HIV-uninfected women in both 2004


and 2011 (Table 1). A subanalysis by
hospitalization type (antenatal/delivery)
showed that mean hospital charges were
higher and mean length of stay was longer
for both delivery and antenatal hospitalizations of HIV-infected, compared with
HIV-uninfected, pregnant women. HIV
infection did not have a signicantly
different effect on length of stay or hospital charges by hospitalization type
(antenatal vs delivery) (data not shown).

hospitalizations
during
pregnancy
per delivery remained higher among
HIV-infected women compared with
HIV-uninfected women in both 2004 and
2011 (1.33 vs 1.11 in 2004 [P < .001];
1.23 vs 1.10 in 2011 [P < .001])
(Table 1). Hospitalizations of pregnant
HIV-infected women were longer (mean
length, 3.64 vs 2.68 days in 2011,
P < .001) and incurred higher hospital
charges (mean charges, $22,980 vs
$14,362 in 2011, P < .001) compared to

TABLE 1

Demographic and hospital characteristics and select outcomes among hospitalizations of pregnant girls and
women aged 15e49 years admitted to US hospitals in 2004 and 2011, by HIV status
2004

2011

Patient/hospital characteristics

HIV infected,
n 7107

HIV uninfected,
n 4,675,615

Age, y

N (%)

N (%)

Pa

488,041 (10.4)

HIV infected,
n 4751

HIV uninfected,
n 4,180,200

N (%)

N (%)

15e19

456 (6.4)

245 (5.2)

359,049 (8.6)

20e34

5622 (79.1)

3,497,064 (74.8)

.007

3631 (76.4)

3,210,178 (76.8)

35e49

1030 (14.5)

690,509 (14.8)

875 (18.4)

610,973 (14.6)

Public

5155 (73.7)

1,886,156 (40.4)

3500 (73.8)

1,865,653 (44.7)

Private

1345 (19.2)

2,514,553 (53.9)

916 (19.3)

2,080,438 (49.9)

Other

496 (7.1)

266,189 (5.7)

326 (6.9)

226,869 (5.4)

1eLowest income

4052 (58.3)

1,300,572 (28.3)

1905 (49.0)

1,122,647 (27.3)

1455 (20.9)

1,120,376 (24.4)

910 (23.4)

1,003,369 (24.4)

920 (13.2)

1,015,807 (22.1)

699 (18.0)

1,097,657 (26.7)

4eHighest income

526 (7.6)

1,160,767 (25.2)

374 (9.6)b

894,705 (21.7)

Rural

320 (4.5)

525,432 (11.2)

168 (3.6)

474,446 (11.5)

Urban

6788 (95.5)

4,150,183 (88.8)

1640 (23.1)

822,720 (17.6)

South
West

Pa
.004

Expected primary payer


<.001

<.001

Median household income quartile for


patient ZIP code
<.001

<.001

Location of hospital
<.001

4491 (96.4)

3,640,248 (88.5)

1422 (29.9)

690,264 (16.5)

952,302 (20.4)

712 (15.0)

858,384 (20.5)

4580 (64.4)

1,703,296 (36.4)

2457 (51.7)

1,580,577 (37.8)

278 (3.9)b

1,197,296 (25.6)

159 (3.4)

1,050,974 (25.1)

<.001

Region
Northeast
Midwest

609 (8.6)

Died during hospitalization

0 (0)

565 (0.01)

Mean length of stay, d

3.63

2.68

Mean hospital charges


Hospitalization/delivery ratio

$14,877
1.33

$10,758
1.11

<.001

e
<.001
<.001
<.001

494 (0.01)
3.64

$22,980
1.23

2.68
$14,362
1.10

<.001

.182
<.001
<.001
<.001

Wald c2; b Estimate should be used with caution-relative SE is >30%; c Suppressed, cell size <10.
Ewing et al. US pregnancy hospitalizations, HIV-infected women: 2004 through 2011. Am J Obstet Gynecol 2016.
a

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Hospitalizations of HIV-infected
pregnant women were more likely than
those of HIV-uninfected pregnant
women to be among older women
(P .004 in 2011), be covered by public
insurance (eg, Medicaid or Medicare)
(P < .001), have listed residences in ZIP
codes with lower median household incomes (P < .001), occur in urban hospitals (P < .001), and occur in the South
and Northeast (P < .001). Frequency of
death during hospitalization was not
different among HIV-infected and
HIV-uninfected pregnant women in
2011 (P .182). No statistical comparison was possible for deaths during hospitalization in 2004 given no recorded
deaths among HIV-infected pregnant
women. Following the general trends
seen in the HIV-uninfected group, mean
hospital charges increased over the study
period for the HIV-infected group, while

length of stay did not change from 2004


through 2011.

Adverse outcomes among


HIV-infected pregnant women
The odds of a diagnosis of several of the
adverse outcomes examined remained
signicantly higher among hospitalizations of HIV-infected pregnant women
compared to HIV-uninfected pregnant
women during 2004 through 2011
(Table 2). In 2011, this included preterm
labor and preterm delivery, preeclampsia
and HTN disorders of pregnancy,
sexually transmitted infections and pelvic inammatory disease, bacterial
infections, nonbacterial infections
(including viral infections, mycoses, and
parasitic infections), and inuenza. A
subanalysis showed that the effect of
HIV infection status on the odds of
bacterial infections was modied by

hospitalization type (delivery/antenatal)


(P < .001). Among antenatal hospitalizations, the odds of bacterial infections
did not differ by HIV status. However,
among delivery hospitalizations, odds of
bacterial infection were signicantly
higher for HIV-infected, compared
with HIV-uninfected, pregnant women
(adjusted odds ratio [aOR], 2.36; 95%
condence interval [CI], 1.71e3.25). In
2004, the odds of GDM were signicantly lower among pregnancy hospitalizations for HIV-infected women
compared to HIV-uninfected women.
However, the rate of GDM in pregnancy
hospitalizations of HIV-infected women
increased signicantly in 2011, such that
there was no difference in the odds of
GDM by HIV status in 2011. The odds
of antepartum hemorrhage in hospitalizations of HIV-infected pregnant
women, compared to hospitalizations of

TABLE 2

Rates of select adverse outcomes among hospitalizations of pregnant women and girls aged 15e49 years
hospitalized in United States in 2004 and in 2011, by HIV status
2004a

2011b

HIV infected, HIV uninfected,


n 7107
n 4,675,615

HIV infected, HIV uninfected,


n 4751
n 4,180,200

Ratec n

Ratec Adjusted odds ratio n

Ratec n

Ratec Adjusted odds ratio

Condition

Preterm labor

1295 24.3

560,187 13.3

1.34 (1.18e1.53)d

795 20.6

447,048 11.7

1.40 (1.16e1.69)d

Preterm delivery

1069 20.0

442,158 10.5

1.41 (1.22e1.63)d

698 18.1

371,156

9.8

1.46 (1.19e1.79)d

217,019

0.61 (0.44e0.85)e

253

6.6

258,194

6.8

1.01 (0.74e1.38)e

94

2.5

13,810

Gestational diabetes

203

3.8

5.2

0.17 1.10 (0.64e1.88)

0.36 1.42 (0.75e2.68)f

Liver disorders

104

2.0

7106

Preeclampsia/hypertension

728 13.6

400,269

9.5

1.08 (0.86e1.35)e

727 18.9

Antepartum hemorrhage

124

2.3

102,355

2.4

0.54 (0.34e0.85)e

139

3.6

85,634

2.3

Major puerperal infection

174

3.3

30,907

0.74 1.24 (0.65e2.36)e

105

2.7

25,260

0.66 0.95 (0.48e1.89)e

Urinary tract infection

422

7.9

132,214

3.1

1.58 (1.18e2.13)g

205

5.3

97,785

2.6

203

5.3

37,856

0.99 3.81 (2.53e5.76)g

205

5.3

42,947

1.1

2.85 (1.84e4.40)h

1225 31.2

160,206

4.2

5.69 (4.20e7.70)h

Sexually transmitted infection,


pelvic inflammatory disease

268

5.0

43,963

1.1

2.58 (1.96e3.40)

Bacterial infection

145

2.7

56,785

1.4

1.36 (0.94e1.97)h

2.3

Viral, mycoses, parasitic


infections
Influenza

1060 19.9
119

2.2

95,422
9440

5.40 (4.46e6.54)

0.22 4.72 (2.88e7.76)h

102

2.6

435,136 11.4

11,854

1.44 (1.16e1.80)e
1.35 (0.995e1.82)e
1.41 (0.97e2.05)g

0.31 4.87 (3.04e7.80)h

In 2004: 5339 deliveries among HIV-infected and 4,204,717 deliveries among HIV-uninfected women; In 2011: 3855 deliveries among HIV-infected and 3,807,760 deliveries among HIVuninfected women; c Rates are per 100 deliveries; d Adjusted for age, primary payer, median household income quartile, hospital location, region, smoking, alcohol use, drug use, anemia,
preeclampsia/hypertension, urinary tract infection, and sexually transmitted infection/pelvic inflammatory disease; e Adjusted for age, primary payer, median household income quartile, hospital
location, region, smoking, alcohol use, drug use, anemia, urinary tract infection, and sexually transmitted infection/pelvic inflammatory disease; f Adjusted for age, primary payer, median household
income quartile, hospital location, region, smoking, alcohol use, drug use, anemia, urinary tract infection, hepatitis B and C, and sexually transmitted infection/pelvic inflammatory disease;
g
Adjusted for age, primary payer, median household income quartile, hospital location, region, smoking, alcohol use, and drug use; h Adjusted for age, primary payer, median household income
quartile, hospital location, region, smoking, alcohol use, drug use, and anemia.
Ewing et al. US pregnancy hospitalizations, HIV-infected women: 2004 through 2011. Am J Obstet Gynecol 2016.

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HIV-uninfected pregnant women, were


signicantly lower in 2004 but borderline higher in 2011. There was no difference in the odds of liver disorders
according to HIV status in either year
studied.
The conditions for which there were
signicant increases in odds among
hospitalizations of HIV-infected pregnant women in 2011, compared with
2004 (Table 3), were GDM (aOR, 1.81;
95% CI, 1.16e2.84), preeclampsia/HTN
disorders of pregnancy (aOR, 1.58; 95%
CI, 1.12e2.24), and 2 categories of
infection diagnoses: viral, mycotic, and
parasitic infections (aOR, 1.90; 95% CI,
1.69e2.14) and bacterial infections
(aOR, 2.54; 95% CI, 1.53e4.20). The
latter category was the only one for which
the increase from 2004 through 2011
among hospitalizations of HIV-infected
women signicantly differed in magnitude from that among HIV-uninfected
women (P value < .001). Odds of preterm labor and preterm birth diagnoses
did not increase for hospitalizations of
HIV-infected pregnant women over the
study period. The trends for preterm labor in the 2 groups were not signicantly
different (P value: .377).

Comment
With this analysis of multiple years of
nationally representative US hospitalization data, we found that the estimated
numbers of hospitalizations and deliveries for HIV-infected pregnant
women did not increase from 2004
through 2011. The rates and adjusted
odds of several morbidities and adverse
pregnancy outcomes remained signicantly higher among hospitalizations of
HIV-infected women compared with
HIV-uninfected women, consistent with
a previously published analysis that
spanned 1994 through 2003.31
To our knowledge, the estimated
number of deliveries to HIV-infected
women in the United States has not
been reported since 2006, and our estimates represent a departure from trends
reported previously, which indicated
that they were increasing from 2000
through 2006.9 This apparent plateau in
number of deliveries to HIV-infected
women is despite wider availability of

new treatments and the demonstrated


effectiveness of perinatal HIV infection
prevention.9,37,38 Studies have shown
that a large majority of pregnancies
among HIV-infected women are unplanned39,40; further, research on longacting contraceptive use among
HIV-infected women from 1998
through 2010 did not show a signicant
increase.41 Our ndings may indicate
that efforts to prevent unintended pregnancy may have some impact in this
population. Hospitalizations of HIVinfected pregnant women tended to
cluster in certain geographic regions,
particularly the South and Northeast.
Pregnancy hospitalizations among HIVinfected women were longer and cost
signicantly more than hospitalizations
of HIV-uninfected pregnant women.
The expected payer for hospitalizations
of HIV-infected women was mostly
Medicaid, consistent with the previous
period studied. While the sampling
scheme of the NIS cannot guarantee that
the included discharges are perfectly
nationally representative of discharges
for a selected condition, it does ensure
that the hospitals from which included
discharges originate are nationally
representative according to the stratication variables. The relationship of
some of these variables to pregnancy
hospitalizations
of
HIV-infected,
compared
with
HIV-uninfected,
women is shown in Table 1.
The odds of adverse outcomese
including preterm labor, preterm delivery, and many categories of
infectionsefor hospitalizations of HIVinfected pregnant women remain
elevated, compared with hospitalizations
of HIV-uninfected pregnant women,
consistent with the previous period.31
Among hospitalizations of HIVinfected pregnant women, no adverse
condition studied showed a statistically
signicant decrease in odds from 2004
through 2011. One encouraging result is
the lack of elevated rates of hospitalizations with liver disorders among pregnant HIV-infected women, despite
concerns about ARV toxicity. From 2004
through 2011, hospitalizations with a
diagnosis of GDM and with preeclampsia/HTN disorders have increased

Original Research

among HIV-infected pregnant women,


mirroring increases of similar magnitude among hospitalizations of HIVuninfected pregnant women. This
increase in the rate of GDM continues a
trend observed from 1994 through
2003.31 Factors such as increased
obesity42-44 or more advanced maternal
age,43,45,46 as well as more sensitive
screening and diagnostic practices47,48
may account for these changes. The
rates of hospitalizations with a diagnosis
of GDM were very similar in 2011 between HIV-infected and HIV-uninfected
women. The odds of urinary tract
infection for pregnancy hospitalizations
of HIV-infected pregnant women were
higher compared with HIV-uninfected
pregnant women in 2004 and not
signicantly different in 2011; this condition did not show a signicant change
over time within the HIV-infected
group.
The more recent period studied saw
the emergence of new ARV agents and
changes to recommendations to include
all HIV-positive pregnant women as
candidates for cART.49-53 Despite these
changes, HIV-infected pregnant women
experienced increases from 2004
through 2011 in hospitalizations for 2
categories of infection, including bacterial and viral/mycotic/parasitic infections. This contrasts with 1994
through 2003, when rates of bacterial
infections did not increase among hospitalizations of HIV-infected pregnant
women.31 Whereas the increase in viral/
mycotic/parasitic diseases was consistent
with a corresponding increase among
hospitalizations of HIV-uninfected
pregnant women, and could thus be
attributed to better screening/diagnosis
or coding practices, the increase in bacterial infections was specic for
HIV-infected pregnant women. The
possibility remains that in more recent
years, more caution is exercised when
coding for infections among HIVinfected women. However, this nding
is unexpected and concerning. Population data from developed countries on
such trends during pregnancy are
limited, but some evidence suggests severe infections during pregnancy may be
increasing.54,55 Since the association

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TABLE 3

Outcomes among hospitalizations of HIV-infected and HIV-uninfected pregnant women and girls aged 15e49 years
in 2007 and 2011 compared to 2004 (adjusted for age group, primary payer, and delivery status)
Year
Tahun
2004
[Referent for OR]

2007
OR (95% CI)

2011
OR (95% CI)

Wanita
terinfeksi
HIV-infected
womenHIV
Persalinan
Prematur
Preterm
labor
a
a
Kelahiran
Prematur
Preterm
delivery

1.11 (0.81e1.52)

0.89 (0.72e1.10)

1.06 (0.80e1.41)

0.98 (0.78e1.24)

Diabetes
GestationalGestasional
diabetes

1.82 (1.18e2.80)

1.81 (1.16e2.84)

Gangguan
Hati
Liver disorders

1.12 (0.58e2.17)

1.35 (0.76e2.39)

Preeklampsia/Hipertensi
Preeclampsia/hypertension

1.08 (0.78e1.49)

1.58 (1.12e2.24)

Pendarahan
Antepartum
Antepartum hemorrhage

1.27 (0.76e2.14)

1.70 (0.98e2.95)

Infeksipuerperal
Puerperium
Mayor
Major
infection

0.51 (0.26e1.00)

0.95 (0.49e1.84)

Urinary tract
infection
Infeksi
Saluran
Kemih

1.08 (0.72e1.61)

0.84 (0.51e1.38)

Infeksi
Seksual,
Penyakit
Radang
SexuallyMenular
transmitted
infection,
pelvic inflammatory
disease
Panggul
Infeksi
BacterialBakteri
infectionbb

1.18 (0.77e1.79)

1.25 (0.72e2.17)

1.86 (1.15e3.01)

2.54 (1.53e4.20)

Infeksi
Virus/ Jamur/
Viral, mycoses,
parasiticParasit
infections

1.28 (1.15e1.42)

1.90 (1.69e2.14)

Influenza
Influenza

1.25 (0.67e2.33)

Mortalitas
rawat inap c,d
Inpatient mortality
c,d rata
Perubahan
rata
Mean charges
Rasio
Rawat inap/ persalinan
Hospitalization/delivery
ratioe,f e,f

$14,904
1.33

1.53 (0.76e3.08)

$17,806

$22,456

1.27

1.23

Persalinan
Prematur
Preterm labor

0.96 (0.90e1.01)

0.89 (0.84e0.95)

a
a
Kelahiran
Prematur
Preterm
delivery

0.98 (0.92e1.04)

0.93 (0.88e1.00)

Diabetes Gestasional
Gestational
diabetes

1.20 (1.13e1.26)

1.34 (1.26e1.42)

Wanita yang tidak


terinfeksi HIV
HIV-uninfected
women

Liver
disorders
Gangguan
Hati

1.35 (1.18e1.54)

2.20 (1.95e2.50)

Preeclampsia/hypertension
Preeklampsia/Hipertensi

1.05 (1.00e1.11)

1.25 (1.18e1.33)

Pendarahan
Antepartum
Antepartum hemorrhage

0.93 (0.89e0.98)

0.94 (0.89e1.00)

Infeksipuerperal
Puerperium
Mayor
Major
infection

0.85 (0.73e0.99)

0.95 (0.79e1.15)

Infeksi tract
Saluran
Kemih
Urinary
infection

0.91 (0.83e0.99)

0.86 (0.79e0.95)

Infeksi
Seksual,
Penyakit
Radang
SexuallyMenular
transmitted
infection,
pelvic inflammatory
Panggul
disease
b
Infeksi
BacterialBakteri
infectionb

0.98 (0.85e1.13)

0.99 (0.84e1.16)

0.92 (0.76e1.11)

0.88 (0.73e1.06)

Infeksi
Virus/ Jamur/
Viral,
mycoses,
parasiticParasit
infections

1.29 (0.95e1.76)

2.01 (1.47e2.77)

Influenza
Influenza

1.10 (1.00e1.21)

1.51 (1.38e1.65)

Mortalitas
rawat inap c,d
Inpatient mortality

1.00 (0.76e1.31)

c,g
Perubahan
rata
rata
Mean
charges

$10,763

Rasio
Rawat inap/ persalinan
Hospitalization/delivery
ratioe,h

e,f

1.11

$12,157
1.10

1.00 (0.74e1.34)
$14,363
1.10

CI, confidence interval; OR, odds ratio.


Preterm delivery logistic regression model adjusted for age and primary payer only; b P value for interaction term testing whether change from 2004 through 2011 differed by HIV status is <.001;
c
Linear regression analysis adjusted for age group, primary payer, and delivery status; d P value for analysis of variance test for mean charges over study period is .002 among HIV-infected women;
e
Ratio of number of hospitalizations to number of deliveries; f P value for comparison in hospitalization delivery ratio from 2004 through 2011 is .04 among HIV-infected women; g P value for
analysis of variance test of variation in mean charges over study period is <.001 among HIV-uninfected women; h P value for comparison in hospitalization delivery ratio from 2004 through 2011 is
.003 among HIV-uninfected women.
Ewing et al. US pregnancy hospitalizations, HIV-infected women: 2004 through 2011. Am J Obstet Gynecol 2016.
a

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OBSTETRICS

between HIV status and bacterial infection was mainly seen in delivery hospitalizations, it may have implications for
the intrapartum management of women
with HIV infection (ie, use of intrapartum antibiotic prophylaxis in select
groups).
Limitations of our study include those
common to research using administrative data. In the HCUP NIS in any year,
there may be multiple observations for
the same patient, as the unit of study is
the hospital admission. This, however,
should not affect delivery estimates for
each year. Medical and coding practices
change over time, affecting trend estimates. Information such as race, previous obstetric history, ARV use, and
obesity, which might affect certain
pregnancy outcomes, is not available.
Race and ethnicity in particular likely
inuences these results, as African
American, and to a lesser extent Hispanic and Latino, women are more likely
to be living with HIV than are
non-Hispanic white women.56 While
evidence on racial and ethnic birth disparities is mixed, it is clear that African
American women have higher rates of
adverse pregnancy outcomes such as
preterm birth,57 and higher maternal
morbidity and mortality than do nonHispanic white women.58,59 Strengths
of this analysis include the large sample
size and the ability to produce nationally
representative estimates, as well as the
availability of cost and length of stay data
to describe the hospitalization burden
on the target population. The ZIP code
income variable provided additional
information about socioeconomic status
that was previously unavailable. An
additional strength of the study is the
relative stability in management recommendations for HIV-infected pregnant
women over the time period under
investigation, in comparison to the prior
article, which spanned pre-highly active
ARV therapy and highly active ARV
therapy eras.
In conclusion, our results demonstrate that HIV-infected pregnant
women in the United States continue
to be at higher risk for many adverse
pregnancy outcomes compared with
HIV-uninfected women. No further

decreases were observed for any of the


morbidities since the end of the previous
study period in 2003; in contrast, there
were increasing trends for some of the
adverse outcomes, such as GDM, HTN
disorders of pregnancy, and infections.
This is despite the wide availability of
effective ARVs, suggesting that availability of effective treatments may not be
sufcient to fully address the health
issues of this population. In addition to
their chronic infection, HIV-infected
women in the US face socioeconomic
disadvantages, which may account, at
least in part, for several of the health
disparities noted. Concerted and creative
efforts are needed to improve the pregnancy outcomes and overall health of
HIV-infected pregnant women. Providers need to be aware that this population remains at risk for several
morbidities during pregnancy, and their
care should be tailored accordingly. n
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Author and article information


From the Division of Reproductive Health, National Center for
Chronic Disease Prevention and Health Promotion, Centers
for Disease Control and Prevention, Atlanta, GA (all authors).
Received May 26, 2016; revised May 26, 2016;
accepted May 26, 2016.
The authors report no conflict of interest. The findings
and conclusions in this report are those of the authors and
do not necessarily represent the views of the Centers for
Disease Control and Prevention.
Presented at the Conference on Retroviruses and
Opportunistic infections (CROI) 2016, organized by
the CROI Foundation and International Antiviral
SocietyeUSA, in Boston, MA, Feb. 22-25, 2016.
Corresponding author: Alexander C. Ewing, MPH.
yhy4@cdc.gov

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