The Journal of Maternal-Fetal and Neonatal Medicine, September 2009; 22(9): 759764

A piece in the puzzle of intrauterine fetal death: Pathological findings in

placentas from term and preterm intrauterine fetal death pregnancies

HILA AMIR1, ADI WEINTRAUB1, BARAK ARICHA-TAMIR1, LIAT APEL-SARID2,

J Matern Fetal Neonatal Med Downloaded from informahealthcare.com by The University of Manchester on 12/19/14

GERSHON HOLCBERG1, & EYAL SHEINER1

1
Department of Obstetrics and Gynecology and 2Department of Pathology, Faculty of Health Sciences, Soroka University
Medical Center, Ben-Gurion University of the Negev, Beer-Sheva, Israel

(Received 23 July 2008; revised 11 September 2008; accepted 17 December 2008)

Abstract
Objective. To compare pathological findings of placentas from term and preterm pregnancies complicated by intrauterine
fetal death (IUFD).
Study design. A retrospective cohort study was conducted including deliveries complicated by IUFD. A comparison was
For personal use only.

made between placentas from term and preterm (537 weeks gestation) pregnancies complicated by IUFD. A second
analysis was undertaken comparing IUFD placentas delivered before and after 34 weeks gestation. Uteroplacental
insufficiency was defined when one or more of the following pathological features were found: placental infarct, poor
vascularity of the chorionic villi, intravascular thrombi and vascular occlusion.
Results. During the study period, 849 placentas of IUFD were examined. Gross and microscopic pathological finding were
noted. When comparing gross and microscopic findings in term and preterm (537 weeks) IUFD placentas, higher rates of
calcifications, tissue congestion and cellular metaplasia were found in term vs. preterm placentas. Significantly increased
rates of poor tissue vascularity, placental vascular occlusion and uteroplacental insufficiency were demonstrated in preterm
IUFD placentas. When comparing pathological findings in IUFD placentas delivered before and after 34 weeks gestation,
higher rates of abnormal cord insertion, calcifications, tissue congestion, infarcts and intravascular thrombi as well as poor
tissue vascularity and placental vascular occlusion were demonstrated in IUFD placentas delivered before 34 weeks.
Regardless of gestational age at the time of IUFD in more than 90% of placentas vascular wall thickening was found. A third
of both term and preterm placentas demonstrated histological chorioamionitis.
Conclusions. A vast majority of IUFD placentas reveal numerous pathological findings that reflect uteroplacental
insufficiency and abnormal blood supply. Different characteristics were noted in term and preterm placentas of pregnancies
complicated by IUFD. Better definition of causes and associated placental pathological findings of IUFD might aid
clinicians in counseling such patients regarding the reason and risk of recurrence in subsequent pregnancies.

Keywords: Intrauterine fetal death, placenta, uteroplacental insufficiency, poor vascularity, vascular occlusion, intravascular
thrombi, infarct

uted to better reporting practices but it could also

Introduction
Intrauterine fetal death (IUFD) is a devastating
occurrence, yet sadly it is not rare in every obstetrical
ward. Because of improved medical care during the
last decade the rate of fetal death has decreased
substantially in the developed world [13]. Never-
theless, Smith and Fretts [4] reported a significant
increase in stillbirth rates since 2001 in England,
Wales and Northern Ireland. This could be attrib-
reflect an increase in prevalence of risk factors [4].
According to the World Health Organisation
(WHO), IUFD is defined as pregnancy loss after
20 completed weeks of gestation or birth weight of
500 g or more [5]. Others advocate the use of 24
weeks (UK) or 28 weeks defined by the border of
viability, in different centers [6]. In Soroka Medical
Center, according to the guidelines of the Ministry of
Health in Israel, IUFD is defined as pregnancy loss

Correspondence: Adi Weintraub, MD, Department of Obstetrics and Gynecology, Soroka University Medical Center, POB 151 Beer-Sheva 84101, Israel.
Tel: 972-8-640-0774. Fax: 972-8-627-5338. E-mail: adiyehud@bgu.ac.il
ISSN 1476-7058 print/ISSN 1476-4954 online 2009 Informa UK Ltd.
DOI: 10.3109/14767050902929396
 760 H. Amir et al.
after 22 complete gestational weeks or a fetus
weighing more than 500 g.
In the United States, the incidence of fetal death is
6.4/1000 births (2002), whereas among Afro-Amer-
ican population it was 12.1/1000, and among
Caucasians 5.5/1000 births. Fetal death consists of
60% of all perinatal death [1]. In Israel, at our center,
the incidence of IUFD was found to be 3.6 per 1000
births [7]. Less then one percent (0.9%) suffered
recurrent perinatal mortality [3].
Many causes and risk factors for IUFD have been
elaborately described in the literature [13,79].
J Matern Fetal Neonatal Med Downloaded from informahealthcare.com by The University of Manchester on 12/19/14
They can be classified to etiologies related to the
fetus, the mother and the pregnancy. In the absence of
a definite cause, many of these cases are defined as
unknown or idiopathic. Furthermore, the causes and
risk factors for fetal death change according to the time
of death. According to Kunzel and Misselwitz [10],
40% of all cases of fetal death occur during week 37 of
gestation or more and 27% occur between weeks 32
and 36. They also found that out of all pregnancies,
the chance of fetal death declines as the pregnancy
continues. In the same study, the main risk factors
found for fetal loss before 36 weeks of gestation were
bleeding because of placenta previa and placental
For personal use only.
abruption. The main risk factors for fetal death beyond
36 weeks of gestation were placental insufficiency,
proteinuria, and diabetes [10].
Comprehensive IUFD assessment is important,
cost-effective and justified for recurrence risk estima-
tion, prenatal diagnosis recommendations, or pre-
conceptual, prenatal, perinatal or neonatal
treatment. Michalski et al. [11] found that when
comprehensive, nonselective analysis is performed,
new and relevant information arises in 51% of IUFD
infants [11]. Upon investigating possible explana-
tions for IUFD, an autopsy is considered the best
possible method. An autopsy can provide informa-
tion regarding the risk factors and offer explanations
for the fetal death, such as chromosomal abnormal-
ities, structural abnormalities, metabolic abnormal-
ities, signs of hypoxia, infection and other
abnormalities. The autopsy result can also aid in
consulting the parents and assessing the odds of
recurrence in 2651% of the cases [12].
Unfortunately, an autopsy is preformed in less
than 50% of the cases mainly because of religious
and cultural reasons in Israel as well as in other
countries in the world. After an autopsy, the most
informative investigation is an examination of the
placenta by a trained pathologist. A macroscopic and
microscopic examination could reveal many patho-
logical findings including structural abnormalities,
infections and evidence of uteroplacental insuffi-
ciency [1,13].
Definitions for preterm, term and post term have
been specifically classified. However, definitions for
subgroups of infants within these categories have not
been well defined. More accurate definitions for the
subgroup of infants born near-term are important
because of the rapid increase in rate of births
attributed to this group. Replacing near-term with
late preterm would better reflect the higher risk for
complications of prematurity experienced by this
subgroup of infants. Late preterm has been defined
as beginning on the 239th day (34 0/7 weeks
gestation) and ending on the 259th day (36 6/7
weeks gestation) since the first day of the last
menstrual period [14].
The literature regarding placental pathologies in
cases of IUFD according to the time of occurrence is
scarce. Little is known about different placental
features in cases of IUFD at term and preterm. The
purpose of this study was to compare pathological
findings in placentas from term and preterm preg-
nancies complicated by IUFD and to assess weather
different pathological features of IUFD placentas
delivered before and after 34 weeks are noted.
Materials and methods
A retrospective cohort study was conducted includ-
ing all singleton deliveries complicated by IUFD,
defined as pregnancy loss after 22 complete gestation
weeks or 500 g. Deliveries occurred between the
years 1995 and 2004 at the Soroka University
Medical Center. This is the sole hospital in the
Negev, the southern part of Israel, serving the entire
obstetrical population in this region. The local ethics
institutional review board approved the study.
Data were collected from the computerised
perinatal database, which includes information pro-
vided immediately after delivery by the attending
obstetrician. Specialist medical secretaries examine
the information routinely before entering it into the
database. Coding is done after assessing the medical
prenatal care records as well as the regular hospital
documents. These procedures ensure the complete-
ness and accuracy of the database.
Pathology data were collected from the compu-
terised pathology database. The placentas at the
pathology department are grossly examined by a
resident in surgical pathology, who routinely takes
two samples from the placental tissue, one sample of
umbilical cord, and one sample of the extra-placental
membranes for each case. Additional tissue is taken
from each gross lesion.
The following clinical characteristics were evalu-
ated: Maternal age, gravidity, parity, ethnicity (Jew-
ish vs. Bedouin Arabs), nulliparity, gestational age,
placental weight. In addition, fetal gender, birth
weight [grouped into small for gestational age
(SGA), appropriate for gestational age (AGA) and
large for gestational age (LAG)], maternal blood type
and Rhesus (Rh) status and maternal serum hemo-
globin level were recorded.
 Placental findings in IUFD pregnancies 761

The following macroscopic pathological features
have been inspected: Placental size and weight,
umbilical cord length and color, number of blood
vessels in the cord, placental tissue engorgement,
infarcts, calcifications and signs of hemorrhage. The
following microscopic features have been examined:
Degree of vascularity, infarcts, placental calcifica-
tions, changes in blood vessel walls and lumen,
thromboses, metaplasia, syncitial knots, hemorrhage,
chorioamnionitis and funisitis.
We defined uteroplacental insufficiency when one
or more of the following pathological features were
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Term IUFD were of higher parity compared with
preterm IUFD. There were no significant differences
between groups neither in maternal age, maternal
blood type and Rh status nor in fetal gender.
Table III presents gross pathological findings in
term and preterm IUFD placentas. Higher rates of
calcifications and tissue congestion were noted in
term as compared with preterm IUFD placentas.
Microscopic pathological findings in term and
preterm IUFD placentas are presented in Table IV.
A significant difference in cellular metaplasia was
found between the groups (70.8% of term IUFD vs.

found: placental infarct, poor vascularity of the
chorionic villi, intravascular thrombi and vascular
occlusion (described elsewhere [15]).
Statistical analysis was performed using the SPSS
package (SPSS, Chicago, IL). Statistical significance
was ascertained using the Chi-square test for
differences in qualitative variables and the Student
t-test for differences in continuous variables. A p-
value of 50.05 was accepted as statistically signifi-
cant.
Results
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55.5% of preterm IUFD, p 0.014). An increased
rate of poor tissue vascularity (86.5% vs. 65.9%,
p 5 0.001), vascular occlusion (25.5% vs. 13.5%,
p 0.022) and uteroplacental insufficiency 83.1% vs.
92.0%, p 0.025) was demonstrated in preterm
IUFD placentas.
Regardless of gestational age at the time of IUFD
in more than 90% of placentas vascular wall
thickening was found. A third of both term and
preterm (537 weeks) placentas demonstrated histo-
logical chorioamionitis.
Table V presents gross pathological findings in
IUFD placentas delivered before and after 34 weeks.

During the study period, 849 placentas of IUFD Higher rates of calcifications and tissue congestion
were examined, macroscopic and microscopic patho- were noted in IUFD placentas delivered after 34
logical finding were noted. Demographic and clinical weeks (29.2% vs. 14.0%, p 5 0.001 and 74.4% vs.
characteristics of patients with term and preterm
IUFD are presented in Table I. Patients were more
likely to be of Bedouin than of Jewish ethnicity Table II. Maternal, fetal and placental characteristics in preterm
and term IUFD.
(62.9% vs. 37.1%). More than 20% of the patients
were nulliparas. Preterm Term
Maternal, fetal and placental characteristics in Characteristics IUFD IUFD p
term and preterm IUFD are presented in Table II.
Maternal age (years + SD) 16.2 + 12.9 29.9 + 0.5 0.52
Biophysical characteristics such as birth-weight for
Gravidity 4.4 + 0.1 4.8 + 0.2 0.89
gestational age, placental volume (ml), placental Parity 3.7 + 0.1 4.3 + 0.2 0.012
weight (g) and length of the placental portion of Maternal blood type 0.57
the cord (cm) are gestational age related and A 30.4 31.6
therefore, were significantly different between B 24.2 23.6
AB 4.8 7.1
groups. A significant higher level of maternal
O 40.5 37.8
hemoglobin was noted in term vs. preterm IUFD Rhesus status 0.29
(11.5 + 0.1 g/dl vs. 11.1 + 0.07 g/dl, p 0.004). Positive Rh 88.5 85.8
Negative Rh 11.5 14.2
Table I. Demographic and clinical characteristics of patients with Maternal serum 11.1 + 0.07 11.5 + 0.1 0.004
IUFD. hemoglobin level (g/dl)
Fetal gender 0.72
Characteristic Study group (n) Male 49.9 51.3
Female 50.1 48.7
Maternal age 29 + 6.87 (849) Birth-weight for gestational age 50.001
Gravidity 4.49 + 3.40 (849) SGA 27.9 35.1
Parity 3.85 + 3.00 (849) AGA 67.9 54.1
Ethnicity LGA 4.2 10.8
Jewish 37.1% (315) Placental volume (ml) 379 + 12 567 + 6 50.001
Bedouins 62.9% (534) Placental weight (g) 413 + 14 831 + 60 50.001
Nulliparity 21.2% (180) Cord length (cm) 26.3 + 0.5 34.6 + 1.0 50.001
Gestational age 31.67 + 5.68 (849)
Placental weight 547.57 + 586.688 (749) SGA, small for gestational age; AGA, appropriate for gestational
age; LGA, large for gestational age.
IUFD, intrauterine fetal demise. Data are expressed as means + standard deviation (SD) or
Data are expressed as mean + standard deviation (SD). percentages.
 762 H. Amir et al.

Table III. Gross pathological findings from preterm and term Table V. Gross pathological findings from IUFD placentas
IUFD placentas. delivered before and after 34 weeks gestation.

Preterm Gross IUFD IUFD

Gross pathological (537weeks) Term pathological before after
finding IUFD IUFD p finding 34 weeks 34 weeks p

Abnormal cord insertion 1.9% (9) 4.1% (7) 0.148 Abnormal cord 1.1% (4) 4.5% (12) 0.006
Calcifications 15.8% (81) 33.5% (59) 50.001 insertion
SUA 5.5% (27) 4.1% (7) 0.455 Calcifications 14% (57) 29.2% (83) 50.001
Meconium 40.4% (21) 36.4% (8) 0.746 SUA 5.2% (20) 5.1% (14) 0.997
Congestion 51.6% (210) 77.3% (116) 50.001 Meconium 55% (22) 67.6% (23) 0.267
Hemorrhage 5.4% (28) 5.7% (10) 0.906 Congestion 47.6% (157) 74.4% (169) 50.001
Infarcts 15.2% (78) 13.6% (24) 0.620 Hemorrhage 5.7% (23) 5.3% (15) 0.828
Infarcts 14% (57) 15.8% (45) 0.511
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IUFD, intrauterine fetal demise.

Data are presented as percentages (n) and p values for statistical IUFD, intrauterine fetal demise.
significance. Data are presented as percentages or means + SD and p values for
statistical significance.

Table IV. Microscopic pathological findings from preterm and

term IUFD placentas. Table VI. Microscopic pathological findings from IUFD placentas
delivered before and after 34 weeks gestation.
Microscopic Preterm
pathological (537weeks) Term Microscopic IUFD IUFD
finding IUFD IUFD p pathological before after
finding 34 weeks 34 weeks p
Poor vascularity 86.5% (160) 65.9% (56) 50.001
Metaplasia 55.5% (111) 70.8% (63) 0.014 Poor vascularity 86.2% (125) 72.8% (91) 0.015
Infarcts 44% (88) 53.9% (48) 0.118 Metaplasia 57.1% (89) 63.9% (85) 0.235
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Vascular occlusion 25.5% (51) 13.5% (12) 0.022 Infarcts 41% (64) 54.1% (72) 0.026
Intravascular thrombi 4.5% (9) 9% (8) 0.134 Vascular occlusion 28.8% (45) 13.5% (18) 0.005
Knots 4.5% (9) 3.4% (3) 0.657 Intravascular thrombi 3.2% (5) 9% (12) 0.036
Wall thickening 91% (182) 91% (81) 0.998 Knots 3.8% (6) 4.5% (6) 0.778
Hemorrhage 12.5% (25) 16.9% (15) 0.322 Wall thickening 91% (142) 91% (121) 0.989
Calcifications 12.5% (25) 10.1% (9) 0.561 Hemorrhage 12.2% (19) 15.8% (21) 0.376
Histological 33% (66) 30.3% (27) 0.655 Calcifications 12.8% (20) 10.5% (14) 0.546
chorioamnionitis Histological 33.3% (52) 30.8% (41) 0.649
Funisitis 6% (12) 6.7% (6) 0.810 chorioamnionitis
Uteroplacental 92.0% (184) 83.1% (74) 0.025 Funisitis 5.8% (9) 6.8% (9) 0.726
insufficiency* Uteroplacental 91.7% (143) 86.5% (115) 0.154
insufficiency*
IUFD, intrauterine fetal demise.
Data are presented as percentages and p values for statistical IUFD, intrauterine fetal demise.
significance. Data are presented as percentages or means + SD and p values for
*Uteroplacental insufficiency was defined as one or more of the statistical significance.
following: vascular occlusion, poor vascularity, intravascular *Uteroplacental insufficiency was defined as one or more of the
thrombi and placental infarcts. following: vascular occlusion, poor vascularity, intravascular
thrombi and placental infarcts.

47.6%, p 5 0.001, respectively). In addition, abnor-

mal cord insertion was significantly more frequent in
IUFD placentas delivered beyond 34 weeks (4.5%
vs. 1.1%, p 0.006).
Microscopic pathological findings in IUFD pla-
centas delivered before and after 34 weeks are
presented in Table VI. Like in preterm placentas
(537 weeks) an increased rate of poor tissue
vascularity and more than a twofold increased rate
of vascular occlusion were found in IUFD placentas
delivered before 34 weeks (72.8% vs. 86.2%,
p 0.006 and 13.5% vs. 28.8, p 0.005, respec-
tively). In IUFD placentas delivered after 34 weeks, a
higher rate of placental bed infarcts were found
(54.1% vs. 41.0%, p 0.026). Pathological findings
of uteroplacental insufficiency were not significantly
different between the groups in this comparison.
Discussion
The main finding of this study is that a vast majority
of IUFD placentas demonstrate pathological char-
acteristics associated with uteroplacental insuffi-
ciency. Over 90% of preterm (537 weeks) and
over 83% of term IUFD placentas were associated
with uteroplacental insufficiency. This finding is in
accordance with Korteweg et al. [16], who discussed
inadequate spiral artery development and vascular
insufficiency as a major placental cause of death [16].

Although similar rates of uteroplacental insufficiency
were noted in placentas delivered before and after 34
weeks gestation, this difference was not statistically
significant. Perhaps, this indicates a late insult, which
occurs more frequently during the period of late
prematurity.
The maternal and fetal placental vascular trees are
dynamic structures which can be significantly altered
by abnormal development, luminal obstruction and
physical loss of integrity. Inflammatory responses can
develop at the maternalfetal interfaces of the
placenta where organisms enter the placental envir-
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onment, fetal antigens are presented to the adaptive
maternal immune system and ischemic processes
release mediators that can activate the innate
immune system [17].
Different placental lesions were associated with
uteroplacental insufficiency [15,18,19]. In this study,
we defined uteroplacental insufficiency when one or
more of the following pathological features were
found: placental infarct, poor vascularity of the
chorionic villi, intravascular thrombi and vascular
occlusion. Unfortunately, no pathological guidelines
regarding autopsy and placental examination after
IUFD exist [16].
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Placental lesions leading to obstruction of the fetal
circulation are an important cause of adverse
pregnancy outcomes [20]. When sufficiently exten-
sive thrombosis may in some cases, be the conse-
quence of stasis or vascular wall damage. In our
study, we found that poor vascularisation was more
frequent in early compared with late IUFD placen-
tas, both when 37 weeks gestation (65.9% term vs.
86.5% preterm, p 5 0.001), and 34 weeks gestation
(72.8% 434 weeks vs. 86.2% 5 34 weeks,
p 0.006), were used as cutoffs.
The most common cause of stasis is compromised
umbilical blood flow secondary to chronic partial or
recurrent intermittent umbilical cord compression
[21, 22]. We found abnormal cord insertion in 4.5%
placentas of IUFD 434 weeks, and only 1.1% when
IUFD occurred before 34 weeks. It is possible that
abnormal cord insertion predisposes the cord to
chronic or acute compression. Five cases were noted
between 34 and 37 weeks, it is possible that the rate
and severity of cord compression increases with
gestational age.
The most common placental inflammatory lesion
is acute chorioamnionitis caused by micro-organisms
gaining access to the placental membranes and/or
amniotic fluid [22], Chorioamnionitis per se is a
maternal inflammatory response beginning near
venules in the decidua capsularis and in the
subchorionic fibrin above the intervillous space and
subsequently spreading into the adjacent chorion
and amnion. This maternal response is usually
clinically silent and has not been associated with
Placental findings in IUFD pregnancies 763
adverse outcomes in most studies [23]. Redline [24]
found that histological evidence of chorioamnionitis
decreases with gestational age reaching 1015% at
term. Histological chorioamnionitis was documented
in 3033% of all IUFD placentas in the current
study, regardless of gestational age. This high and
constant incidence of histological chorioamnionitis
could be the cause of IUFD in some cases, whereas
in others, it could be the result of a prolonged
induced labour.
Higher rates of calcifications and tissue congestion
were noted in placentas from term IUFD placentas
compared with preterm (537 weeks) placentas. This
was also true while comparing IUFD before and after
34 weeks gestation. Calcifications are common in
human placentas and are widely recognised as a
normal part of maturation and aging of this organ
[25]. Tissue congestion may be a result of stasis and
therefore reflects a consequence rather than a cause
of IUFD. Placental tissue congestion can be a result
of increased resistance to flow through the umbilical
and placental vessels, therefore decreased flow,
venous stasis, villous congestion, and distension of
the fetal vessels, predisposing the placenta to the
development of thrombi and congestion. Lack of
blood flow through fetal vessels could lead to
decreased oxygen to the placenta and fetus, poten-
tially causing intrauterine hypoxia [26].
The lesion of acute atherosis is characterised by
thickening of the vascular intima and necrosis of the
media. Intimal thickening is because of deposition of
fibrin and other plasma constituents and migration of
macrophages and myointimal cells which accumulate
fat in their cytoplasm to become foam cells. Clinical
and experimental studies indicate that these lesions
can be initiated by several factors which cause
endothelial injury [27]. Placental vascular wall
thickening was found in over 90% of placentas
examined in the current study. Because we could not
differentiate between cases in which endothelial
injury was the cause of IUFD from those in which
it was the result of IUFD we did not include this
variable in the definition of placental insufficiency.
Cellular metaplasia occurs because of abnormal
stimulus, such as fetal stress or inflammation, and
includes a replacement of one differentiated cell type
to another, to survive the changing environment
[28]. Such metaplasia was more frequent in term
placentas, which might reflect fetal stress occurring
late in gestation, causing cellular metaplasia and
eventually fetal death.
In conclusion, a vast majority of IUFD placentas
reveal pathological findings that reflect uteroplacen-
tal insufficiency and abnormal blood supply. Differ-
ent characteristic findings were noted in term and
preterm placentas of pregnancies complicated by
IUFD. In future studies, a better definition of IUFD
 764 H. Amir et al.
causes and associated placental pathological findings
might aid clinicians in counseling, assessing the risk
of recurrence and even preventing IUFD in sub-
sequent pregnancies.
Declaration of interest: The authors report no
conflicts of interest. The authors alone are respon-
sible for the content and writing of the paper.
References
1. Silver RM. Fetal death. Obstet Gynecol 2007;109:153167.
J Matern Fetal Neonatal Med Downloaded from informahealthcare.com by The University of Manchester on 12/19/14
2. Fretts RC. Etiology and prevention of stillbirth. Am J Obstet
Gynecol 2005;193:19231935.
3. Weintraub AY, Rozen A, Sheiner E, Levy A, Press F,
Wiznitzer A. Perinatal mortality: a sporadic event or a
recurrent catastrophe? Arch Gynecol Obstet 2009;279:299
303.
4. Smith GC, Fretts RC. Stillbirth. Lancet 2007;370:1715
1725.
5. Johansen KS, Hod M. Quality development in perinatal care
the OBSQID project. OBStetrical quality indicators and data.
Int J Gynaecol Obstet 1999;64:167172.
6. Cartlidge PH, Stewart JH. Effect of changing the stillbirth
definition on evaluation of perinatal mortality rates. Lancet
1995;346:486488.
7. Oron T, Sheiner E, Shoham-Vardi I, Mazor M, Katz M,
Hallak M. Risk factors for antepartum fetal death. J Reprod
For personal use only.
Med 2001;46:825830.
8. Froen JF, Arnestad M, Frey K, Vege A, Saugstad OD, Stray-
Pedersen B. Risk factors for sudden intrauterine unexplained
death: epidemiologic characteristics of singleton cases in Oslo,
Norway, 19861995. Am J Obstet Gynecol 2001;184:694
702.
9. Vintzileos AM, Ananth CV, Smulian JC, Scorza WE, Knuppel
RA. Prenatal care and blackwhite fetal death disparity in the
United States: heterogeneity by high-risk conditions. Obstet
Gynecol 2002;99:483489.
10. Kunzel W, Misselwitz B. Unexpected fetal death during
pregnancy a problem of unrecognized fetal disorders during
antenatal care? Eur J Obstet Gynecol Reprod Biol 2003;110:
S86S92.
11. Michalski ST, Porter J, Pauli RM. Costs and consequences of
comprehensive stillbirth assessment. Am J Obstet Gynecol
2002;186:10271034.
12. Hey EN, Lloyd DJ, Wigglesworth JS. Classifying perinatal
death: fetal and neonatal factors. Br J Obstet Gynaecol
1986;93:12131223.
13. Faye-Petersen OM, Guinn DA, Wenstrom KD. Value of
perinatal autopsy. Obstet Gynecol 1999;94:915920.
14. Engle WA. A recommendation for the definition of late
preterm (near-term) and the birth weight-gestational age
classification system. Semin Perinatol 2006;30:27.
15. Salafia CM, Pezzullo JC, Minior VK, Divon MY.
Placental pathology of absent and reversed end-diastolic flow
in growth-restricted fetuses. Obstet Gynecol 1997;90:830
836.
16. Korteweg FJ, Gordijn SJ, Timmer A, Holm JP, Ravise JM,
Erwich JJ. A placental cause of intra-uterine fetal death
depends on the perinatal mortality classification system used.
Placenta 2008;29:7180.
17. Redline RW. Placental pathology: a systematic approach with
clinical correlations. Placenta 2008;29:S86S91.
18. Salafia CM, Ernst LM, Pezzullo JC, Wolf EJ,
Rosenkrantz TS, Vintzileos AM. The very low birthweight
infant: maternal complications leading to preterm birth,
placental lesions, and intrauterine growth. Am J Perinatol
1995;12:106110.
19. Salafia CM, Minior VK, Pezzullo JC, Popek EJ, Rosenkrantz
TS, Vintzileos AM. Intrauterine growth restriction in infants
of less than thirty-two weeks gestation: associated placental
pathologic features. Am J Obstet Gynecol 1995;173:1049
1057.
20. Redline RW. Severe fetal placental vascular lesions in term
infants with neurologic impairment. Am J Obstet Gynecol
2005;192:452e7.
21. Redline RW. Clinical and pathological umbilical cord
abnormalities in fetal thrombotic vasculopathy. Hum Pathol
2004;35:14941498.
22. Redline RW, Faye-Petersen O, Heller D, Qureshi F, Savell V,
Vogler C. Amniotic infection syndrome: nosology and
reproducibility of placental reaction patterns. Pediatr Dev
Pathol 2003;6:435448.
23. Redline R, Wilson-Costello D, Borawski E, Fanaroff A, Hack
M. The relationship between placental and other perinatal risk
factors for neurologic impairment in very low birth with
children. Pediatr Res 2000;47:721726.
24. Redline RW. Inflammatory responses in the placenta and
umbilical cord. Semin Fetal Neonatal Med 2006;11:296301.
25. Varma VA, Kim KM. Placental calcification: ultrastructural
and X-ray microanalytic studies. Scan Electron Microsc
1985;(Part 4):15671572.
26. Baergen RN, Malicki D, Behling C, Benirschke K. Morbidity,
mortality, and placental pathology in excessively long umbi-
lical cords: retrospective study. Pediatr Dev Pathol 2001;4:
144153.
27. De Wolf F, Brosens I, Robertson WB. Ultrastructure of
uteroplacental arteries. Contrib Gynecol Obstet 1982;9:86
99.
28. Chew RH, Silberberg BK. Possible association of acute
inflammatory exudate in chorioamnionitis and amniotic
squamous metaplasia. Am J Clin Pathol 1990;93:582585.