Original Article

Pregnancy Outcomes in Women with Preeclampsia

Superimposed on Chronic Hypertension with and
without Severe Features
Hind N. Moussa, MD1 Mateo G. Leon, MD1 Ana Marti, MD1 Alissar Chediak, MD1
Claudia Pedroza, PhD2 Sean C. Blackwell, MD1 Baha M. Sibai, MD1

1 Division of Maternal-Fetal Medicine, Department of Obstetrics, Address for correspondence Hind N. Moussa, MD, Department of
Gynecology and Reproductive Sciences, The University of Texas Obstetrics, Gynecology and Reproductive Sciences, University of Texas
Health Science Center at Houston, Houston, Texas Health Science Center at Houston, 6431 Fannin Street, Suite 3.264,
2 Center for Clinical Research and Evidence-Based Medicine, The Houston, TX 77030 (e-mail: Hind.N.Moussa@uth.tmc.edu).
University of Texas Health Science Center at Houston, Houston, Texas

Am J Perinatol

Abstract Objective The American Congress of Obstetricians and Gynecologists (ACOG) task force
on hypertension in pregnancy introduced a new definition of superimposed preeclampsia
(SIP) adding severe features (SF) as new criteria to define severe disease. They also

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recommended that those with SIP be delivered
37 weeks, whereas those with SF be
delivered  34 weeks. Our aim was to investigate the validity of this new definition by
comparing adverse pregnancy outcomes in SIP with (SIP-SF) and without SF (SIP).
Study Design Women with chronic hypertension (CHTN) enrolled in a multicenter trial
were studied. SIP was reclassified according to the new definition to SIP and SIP-SF
(persistent systolic blood pressure [BP] > 160 or diastolic BP > 110, platelets < 100 K,
liver function tests > 70, creatinine > 1.1, or persistent central nervous system/
abdominal symptoms). Composite adverse outcomes including rates of indicated
preterm birth, abruptio placentae, postpartum hemorrhage, and maternal death
were compared by chi-square. Adjustment was done with a multivariate logistic-
regression analysis and all statistical tests were two-sided.
Results A total of 216 women (28%) out of 774 with CHTN developed SIP, 87 (11%) had
SIP-SF, and 129 (17%) didn’t have SF. Baseline characteristics including maternal age,
baseline BP, and assignment to low-dose aspirin were similar between groups. Using
univariate analysis, the composite adverse outcome was higher among the SIP-SF group
(p ¼ 0.04), as well as indicated preterm birth (p ¼ 0.02), cesarean section (p ¼ 0.02),
and SGA (p ¼ 0.02). After adjustment, composite adverse outcomes were not signifi-
Keywords cantly different between groups. The rate of SGA, however, was higher among SIP-SF
► chronic hypertension (adjusted odds ratio: 3.12, p ¼ 0.02).
► superimposed Conclusion The rate of SIP-SF in this study was 11% of all women with CHTN.
preeclampsia Surprisingly, pregnancy outcomes were not significantly different in those with and
► severe features without SF. We suggest a prospective observational study to determine the optimal
► pregnancy outcomes timing for delivery in those with SIP using new ACOG diagnostic criteria.

received Copyright © by Thieme Medical DOI http://dx.doi.org/

June 8, 2016 Publishers, Inc., 333 Seventh Avenue, 10.1055/s-0036-1592134.
accepted after revision New York, NY 10001, USA. ISSN 0735-1631.
July 30, 2016 Tel: +1(212) 584-4662.
Preeclampsia Superimposed on Chronic Hypertension Moussa et al.

Hypertensive disorders in pregnancy complicate up to 10% of • New onset of proteinuria or a sudden increase in protein-
pregnancies worldwide.1 There are 600,000 annual global uria in a woman with known proteinuria before or early in
maternal deaths, and more than 70,000 (12%) are secondary pregnancy.
to preeclampsia and eclampsia.2
Severe maternal outcomes such as stroke-cerebrovascular SIP with SF is defined as CHTN with severe range BPs
complications, pulmonary edema, mechanical ventilation, acute despite treatment and/or in association with symptoms or
renal failure and death are more frequent in chronic hyperten- laboratory abnormalities. These include thrombocytopenia
sion (CHTN) patients as compared with a healthy control group.3 < 100,000 platelets, elevated level of transaminases (double
In addition, several studies have associated CHTN to adverse the upper limit of the normal range), new-onset upper
perinatal outcomes, including preterm birth, intrauterine quadrant pain or epigastric pain or new onset of renal
growth restriction, and perinatal death.4–7 Preeclampsia is insufficiency with serum creatinine > 1.1 mg/dL, doubling
dangerous whether present alone or superimposed on preexist- serum creatinine levels, pulmonary edema, or new onset of
ing CHTN, however, it is well known that maternal and fetal cerebral or visual disturbance.
morbidity dramatically increase when the latter is present.1,8 A primary composite adverse outcome was studied, and
The American Congress of Obstetricians and Gynecologists defined as the presence of indicated preterm birth, abruptio
(ACOG) task force (TF) on hypertension in pregnancy,1 suggests placentae, postpartum hemorrhage, or maternal death. Indi-
that superimposed preeclampsia should be stratified into two vidual components of the composite adverse outcome, as well
groups: SIP and SIP with SF. The distinction of the above entities as other maternal outcomes such as gestational age, route of
is crucial for the management of the patient, especially in regards delivery, and preterm labor were also examined. Perinatal
to timing of delivery as well as the use of magnesium sulfate for outcomes included length of stay in neonatal intensive care
seizure prophylaxis, but their correlation with maternal and unit (NICU), a composite respiratory morbidity (respiratory
neonatal outcomes remains unclear. The purpose of this study is distress syndrome, respiratory support/intubation, or bron-

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to evaluate pregnancy outcomes in pregnancies complicated by chopulmonary disease), and other composite morbidity
superimposed preeclampsia with or without severe features (Apgar < 3 at 5 minutes, neurological outcome including
using the new ACOG TF criteria. seizure, intraventricular hemorrhage > grade 3, retinopathy
of prematurity, or perinatal death). The definitions of the
outcomes and the detailed protocol for the data collection are
Materials and Methods
widely described in the primary article.9 Preterm birth was
We performed a secondary analysis of the Eunice Kennedy defined as delivery before the completion of 37 weeks’ of
Shriver National Institute of Child Health and Human Develop- gestation; indicated preterm births were centrally coded as
ment Maternal-Fetal Medicine Units Network multicenter ran- preterm births resulting from reasons other than spontane-
domized trial evaluating the use of low-dose aspirin for ous labor or premature rupture of membranes. Abruptio
preeclampsia prevention in high-risk pregnancies.9 The primary placentae was diagnosed according to clinical criteria (vaginal
cohort study included 2,539 women considered at high risk for bleeding and uterine tenderness) and examination of
the development of preeclampsia; these were women with the placenta. Preeclampsia was defined as BP elevation
pregestational, insulin-dependent diabetes mellitus, multifetal (BP 140/90 mm Hg or greater on two occasions at least
gestations, preeclampsia in a previous pregnancy, and CHTN. The 4 hours apart in those who were previously controlled) or
diagnosis of CHTN before 20 weeks of gestation required specific worsening hypertension (two diastolic readings greater than
documentation described in detail in the original trial.9 Before 110 mm Hg taken 4 hours apart in the week before delivery)
enrollment, all women between 13th and the 26th week of plus at least one of the following: new proteinuria or a sudden
gestation underwent defined tests to assess for proteinuria and increase in proteinuria (either five times the baseline value or
compliance.9 Enrolled women were randomly assigned to twice the baseline if the baseline value exceeded 5 g/24 h),
receive either 60 mg of aspirin, or an identical in appearance thrombocytopenia (less than 100,000/mm3), a serum aspar-
placebo. Of note, aspirin did not influence the risk of preeclamp- tate aminotransferase (greater than 70 unit/L), symptoms
sia in these patients. Weight, qualitative urinary protein excre- (including severe headache or epigastric pain), eclamptic
tion (measured by dipstick), and blood pressure (BP) were convulsion, HELLP (hemolysis, elevated liver enzymes, and
measured at each visit. Only women with BP over 140/90 mm low platelet count) syndrome, or pulmonary edema. Protein-
Hg at the time of enrollment were considered for this analysis, as uria was defined as excretion of 300 mg of protein in a
well as women with BP measuring less than this value if they 24-hour urine collection or two dipstick test results of greater
were receiving antihypertensive therapy. than 2þ (greater than 100 mg/dL), at least 4 hours apart, with
According to the new recommendations of the ACOG TF on no evidence of urinary tract infection. A neonate was consid-
hypertension in pregnancy,1 superimposed preeclampsia ered small for gestational age (SGA) if its weight was below
should be stratified into two groups: SIP and SIP with SF. the 10th percentile of normative birth weights for singletons.
The following constitutes criteria for SIP: Both the preenrollment BP and the previously mentioned
study outcomes were key variables of the primary trial. These
• A sudden increase in BP that was previously well con- data were abstracted by trained and certified research nurses,
trolled or escalation of antihypertensive medications to entered by trained data abstractors, and securely transmitted
control BP. to the biostatistics coordinating center. To ensure consistency

American Journal of Perinatology

 Preeclampsia Superimposed on Chronic Hypertension Moussa et al.

in the ascertainment of outcomes, particularly preeclampsia women, CHTN women who developed SIP, and CHTN women
and abruption, the records of all the women with suspected who developed SIP with SF.
preeclampsia or abruption were reviewed centrally and For data analysis, comparisons among groups were per-
independently by two to three physicians unaware of the formed using chi-square and Fisher exact tests. Multivariable
treatment group assignments. They had to agree unanimous- logistic regression models were created to estimate the
ly on the validity of the designated outcomes. In addition, the adjusted odds ratio (aOR) and the 95% confidence interval
groups were redefined to fit the definitions according to the (CI) to evaluate the association of SF with the adverse out-
new TF guidelines including the previously discussed CHTN comes of the pregnant population previously described. This

Table 1 Baseline maternal characteristics

Chronic hypertension Superimposed Superimposed p Value

N ¼ 558 preeclampsia preeclampsia with
N ¼ 129 severe featuresa
N ¼ 87
Maternal age (y)
< 35 418 (75) 92 (71) 68 (78) 0.51

35 140 (25) 37 (29) 19 (22)
Parity
Primipara 135 (24) 32 (25) 25 (29) 0.66

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Multipara 423 (76) 97 (75) 62 (71)
Race
Black 333 (60) 83 (64) 53 (61) 0.29
Hispanic 60 (11) 18 (14) 13 (15)
White or other 165 (30) 28 (22) 21 (24)
Marital status
Married/living with partner 217 (39) 59 (46) 36 (41) 0.35
Divorced or other 341 (61) 70 (54) 51 (59)
Gestational age at time of randomization (wk) 19.9  3.8 19.6  3.8 20  3.8 0.59
Gestational age at diagnosis (wk) 14.7  5.8 13.4  6.2 0.17
2
Pre-pregnancy BMI (kg/m )
< 25 124 (22) 24 (19) 16 (19) 0.23
25–29 80 (14) 27 (21) 18 (21)
> 29 350 (63) 75 (60) 51 (60)
Antihypertensive drug use
Started before pregnancy 357 (64) 88 (68) 61 (70) 0.04
Started during pregnancy 68 (12) 21 (16) 15 (17)
None 133 (24) 20 (16) 11 (13)
Baseline proteinuria > 300 mg Hg (24 h)b 51 (18) 10 (12) 15 (31) 0.02
Baseline blood pressure (first visit)
Mean SBP 126.7  14.7 131.9  14.2 131.2  11.9 0.001
Mean DBP 76.4  12 83.3  10.8 80.6  12.4 < 0.001
MAP 93.1  11.6 99.5  10.6 97.4  10.9 < 0.001
Aspirin use 277 (50) 59 (46) 52 (60) 0.12
Tobacco use during pregnancy 141 (25) 26 (20) 21 (24) 0.47
Alcohol use during pregnancy 83 (15) 18 (14) 11 (13) 0.85

Abbreviations: BMI, body mass index; DBP, diastolic blood pressure; SBP, systolic blood pressure; MAP, mean arterial pressure.
a
Severe features include any of the following: Severe range blood pressure/thrombocytopenia < 100,000 per µL/elevated liver transaminases/new
onset and worsening renal insufficiency/pulmonary edema/persistent cerebral or visual disturbances.
b
Different denominator as there were missing data for this variable.

American Journal of Perinatology

Preeclampsia Superimposed on Chronic Hypertension Moussa et al.

model was adjusted for the following potential confounding eclampsia. Among these women, 129 (17%) had SIP without
factors: age, nulliparity, race, body mass index, gestational SF and 87 (11%) had SIP-SF. Baseline characteristics including
age at randomization, hypertension medications before preg- maternal age, baseline BP, and assignment to low-dose aspirin
nancy, hypertension medications started during pregnancy, were similar between both groups (►Table 1). Using univari-
aspirin therapy, smoking, and baseline proteinuria. Statistical ate analysis, gestational age at delivery was found to be lower
significance was considered with a p value of < 0.05. All among the SIP-SF group (CHTN [37.2  4.2] vs. SIP
analyses were performed using STATA, SE version 13.1 statis- [35.3  4.4] vs. SIP-SF [34.3  4.6], p < 0.001). Women
tical software (StataCorp LP, College Station, TX). All Statistical who developed SIP-SF were at higher risk of indicated pre-
tests were two sided. The current study was submitted to the term birth (10 vs. 43 vs. 63%, p < 0.001), cesarean section (30
University of Texas Health Science Center Institutional vs. 40 vs. 56%, p < 0.001), and SGA (9 vs. 13 vs. 20%,
Review Board and was considered exempt. p ¼ 0.007) (►Table 2). The composite adverse outcome was
higher among the SIP-SF group (CHTN [16%] vs. SIP [52%] vs.
SIP-SF [67%], p < 0.001), as well as the neonatal composite
Results
respiratory morbidity (8 vs. 15 vs. 20%, p < 0.001), and other
Out of 2,539 women enrolled in the primary study, 774 neonatal composite morbidity (6 vs. 14 vs. 15%, p < 0.001)
patients had CHTN, and 216 (28%) had superimposed pre- (►Table 3). After adjustment, the composite adverse outcome

Table 2 Maternal and neonatal outcomes in CHTN, SIP, and SIP with severe features

Chronic hypertension Superimposed Superimposed p Value

N ¼ 558 preeclampsia preeclampsia with
N ¼ 129 severe featuresa

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N ¼ 87
Gestational age (wk) 37.2  4.2 35.3  4.4 34.3  4.6 < 0.001
Indicated preterm birth 52 (10) 59 (46) 54 (63) < 0.001
Route of delivery
Vaginal 383 (70) 78 (60) 38 (44) < 0.001
Cesarean 164 (30) 51 (40) 49 (56)
Premature labor 86 (16) 21 (16) 20 (23) 0.24
Abruptio placentae 5 (1) 5 (4) 1 (1) 0.04
Eclampsia 0 (0) 0 (0) 23 (3.01) < 0.001
HELLP 0 (0) 0 (0) 0 (0)
Death 0 (0) 0 (0) 1 (1.15) 0.01
Days of ventilation 2.2  5.3 6.3  14.9 4.1  7.5 0.07
Apgar < 3 at 5 min 21 (4) 5 (4) 6 (7) 0.42
Respiratory morbidity
RDS 9 (10) 3 (6) 4 (11) 0.71
BPD 5 (5) 6 (13) 3 (9) 0.30
Neurologic morbidity
Seizure 4 (4) 3 (6) 0 (0) 0.33
IVH > grade III 1 (0.2) 0 (0) 3 (3.5) < 0.001
ROP 5 (5) 8 (18) 4 (11) 0.07
SGA 48 (9) 16 (13) 17 (20) 0.007
Length of stay in NICU (d) 15.7  21.7 21.2  27.1 23.9  27.9 0.11
Antepartum stillbirth 11 (2) 6 (5) 2 (2) 0.22
Intrapartum stillbirth 1 (0.2) 0 (0) 2 (2.3) 0.01
Neonatal death 7 (1) 5 (4) 3 (3) 0.09

Abbreviations: BPD, bronchopulmonary dysplasia; CHTN, chronic hypertension; CLD, chronic lung disease; IVH, intraventricular hemorrhage; NE,
necrotizing enterocolitis; RDS, respiratory distress syndrome; ROP, retinopathy of prematurity; SGA, small for gestational age; SIP, superimposed
preeclampsia; TTN, transient tachypnea of the newborn.
a
Severe features include any of the following: Severe range blood pressure/thrombocytopenia < 100,000 per µL/elevated liver transaminases/new
onset and worsening renal insufficiency/pulmonary edema/persistent symptoms including central nervous system and epigastric pain.

American Journal of Perinatology

 Preeclampsia Superimposed on Chronic Hypertension Moussa et al.

Table 3 Composite outcomes in CHTN, SIP, and SIP with severe features

Chronic hypertension Superimposed Superimposed p Value

N ¼ 527 preeclampsia preeclampsia with
N ¼ 126 severe featuresa
N ¼ 87
Composite perinatal 86 (16) 65 (52) 54 (67) < 0.001
Neonatal composite respiratory morbidity 42 (8) 19 (15) 17 (20) < 0.001
Other neonatal composite morbidity 32 (6) 18 (14) 13 (15) < 0.001

Abbreviations: aOR, adjusted odds ratio; CI, confidence interval; CHTN, chronic hypertension; SIP, superimposed preeclampsia.
Note: Composite perinatal includes any indicated preterm birth, small for gestational age, abruptio placentae or maternal death.
Neonatal composite respiratory includes respiratory distress syndrome, respiratory support/intubation, and bronchopulmonary dysplasia.
Other neonatal composite includes Apgar < 3 at 5 minutes, neurological outcome including seizure, intraventricular hemorrhage > grade 3,
retinopathy of prematurity, or death.

did not reach significant statistical difference between the SIP dation, and perinatal mortality.14 The risks of SIP on preg-
and SIP-SF group (aOR: 1.3, p ¼ 0.49), however, they were nancy outcomes have also been described; when comparing
significantly different from those in the chronic hypertensive SIP with preeclampsia, one study found no difference in
group (aOR: 12.4, p < 0.001). Similar results were evidenced perinatal outcomes, however, a higher rate of delivery before
with the neonatal composite respiratory morbidity outcome 34 weeks, cesarean delivery, and NICU admissions were
and other composite outcome (►Table 4). After adjustment, noticed.8 On the other hand, there is a paucity of reports

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SGA remained significantly different suggesting a higher rate on the outcomes of pregnant women who develop SIP-SF, and
among patients who developed SIP-SF (aOR: 3.12, p ¼ 0.02). it remains unclear whether these outcomes really differ from
those who develop SIP. After adjusting for confounders, we
found no statistical difference between the rates of composite
Discussion
adverse outcomes, neonatal composite respiratory morbidity,
To our knowledge, this is the first study to report the rate of and other composite neonatal morbidities among the pa-
SIP-SF, as well as the first to compare pregnancy outcomes of tients who developed SIP and SIP-SF. However, both of these
SIP versus SIP-SF according to the new TF definitions. groups were found to have higher rates of all three composite
The reported incidence of SIP in women with CHTN ranges groups when compared with CHTN patients who did not
between 13 and 40%.10–13 The incidence of 28% we obtained develop SIP. After logistic regression, SGA was the only
in our study lies within that range. CHTN was reported to have outcome that was found to be significantly higher among
increased by 80% over a 14-year period, with an expectation patients with SF in comparison to those who had SIP without
that it will continue to increase, as it correlates with the rising SF. Apart from SGA, our data shows no significant differences
advanced maternal age and maternal obesity.3 The preva- in pregnancy outcomes among those with and without severe
lence of SIP-SF was found to be 11%, hence the importance of features, and interprets a higher risk of adverse outcomes for
adequate patient counseling in this common condition. CHTN both conditions when compared with the CHTN population.
alone increases the risk of adverse outcomes such as cesarean According to the new TF recommendations, it is crucial
delivery, postpartum hemorrhage, intrauterine growth retar- to distinguish SIP and SIP with SF as it will affect patient

Table 4 Pregnancy outcomes after adjustment for confounders

aOR (95% CI) p Value aOR (95% CI) p Value aOR (95% CI) p Value
SIP-CHTN SIP with SF-CHTN SIP–SIP with SF
Composite perinatal 9.3 (5.1–16.9) < 0.001 12.4 (5.73–26.79) < 0.001 1.34 (0.59–3.07) 0.49
Neonatal composite 2.95 (1.38–6.33) 0.05 2.84 (1.20–6.78) 0.018 1.04 (0.40–2.71) 0.94
respiratory morbidity
Other neonatal composite 3.43 (1.50–7.88) 0.04 3.14 (1.24–8.0) 0.016 0.92 (0.33–2.53) 0.866
morbidity

Abbreviations: aOR, adjusted odds ratio; CI, confidence interval; CHTN, chronic hypertension; SIP, superimposed preeclampsia.
a
Outcomes after adjustment for age, nulliparity, race, body mass index, gestational age at randomization, hypertension medications before
pregnancy, hypertension medications started during pregnancy, aspirin therapy, smoking, and baseline proteinuria.
Note: Composite perinatal includes any indicated preterm birth, small for gestational age, abruptio placentae or maternal death.
Neonatal composite respiratory includes respiratory distress syndrome, respiratory support/intubation, and bronchopulmonary dysplasia.
Other neonatal composite includes Apgar < 3 at 5 minutes, neurological outcome including seizure, intraventricular hemorrhage > grade 3,
retinopathy of prematurity, or death.

American Journal of Perinatology

Preeclampsia Superimposed on Chronic Hypertension Moussa et al.

management. The use of magnesium sulfate to prevent References

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Conflict of Interest the risk for adverse pregnancy outcome after superimposed pre-
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American Journal of Perinatology