Human Pathology Reports 27 (2022) 300586

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Human Pathology Reports

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Case Report

Utility of fetal autopsy findings to estimate time of intrauterine fetal demise

in maternal trauma
Daniel S. Atherton a, b, *, Brandi C. McCleskey a, b, Virginia E. Duncan a
a
Department of Pathology, University of Alabama-Birmingham, 1670 University Blvd, Birmingham, AL 35233, United States
b
Jefferson County Coroner’s / Medical Examiner’s Office, 1515 6th Avenue South, Birmingham, AL 35233, United States

A R T I C L E I N F O A B S T R A C T

Keywords Forensic pathologists determine cause and manner of death in sudden and unexpected deaths. Fetal autopsies can
Intrauterine fetal demise be challenging because they are rare, fetal death can occur in the context of maternal injuries, and examination
Fetal death findings are usually affected by postmortem changes. We present a case involving a 26 week gestational age fetus
Timing of fetal demise
with intrauterine demise in the context of maternal assault. In the assault, the assailant compressed the abdomen
Intrauterine retention time
of the mother while striking her. The fetus was determined to be dead by ultrasound after the mother arrived at a
Maternal assault
hospital. The fetus was delivered by induction the following day. Examination of the fetus showed mild
maceration, and microscopic examination of various organs showed findings compatible with a fetal death of no
more than 48 h prior to delivery. Taking the circumstances, gross findings, and microscopic findings into ac­
count, the cause of death was determined to be the result of compression of the mother’s abdomen during the
assault. This case highlights the importance of accurate timing of intrauterine fetal demise particularly as it
relates to maternal trauma.

1. Introduction 2. Case presentation

Coroner’s/Medical Examiner’s Offices (CMOs) investigate sudden
and unexpected deaths. This investigation typically includes gathering
information about circumstances surrounding a death and performing
postmortem examinations/autopsies. Medical examiners/forensic pa­
thologists (FPs) rely on all of this information to form their opinions
about cause and manner of death. CMOs assume jurisdiction of any
sudden or unexpected death that occurs in a violent context, and for
most CMOs, this includes the death of fetuses whose deaths could be
from trauma sustained by the mom. The investigation of fetal deaths
presents a great challenge for FPs for a few reasons: fetal deaths in the
context of violence are rare, many modes of maternal violence do not
necessarily translate to visible injuries on the fetus, and various post­
mortem changes invariably take place between a traumatic event, de­
livery, and subsequent examination of the fetus. The case reported here
provides an example of how postmortem examination can reveal gross
and microscopic findings to correlate the timing of fetal death with a
traumatic event.
A pregnant woman was transported to a local hospital after being
assaulted. According to the investigation, on the day of the assault, at
approximately 1100 h, the assailant “sat” on the mother’s abdomen
while striking her. The victim reported the assault, and first responders
arrived at the scene and transported her to the hospital, where she and
her fetus were evaluated. Medical records from the hospital documented
several bruises on the mother, and ultrasound of the fetus at 1520 h
showed absence of fetal heart tones (intrauterine fetal demise; IUFD).
Labor was induced, and a 26 week, 3 day gestational age stillborn fetus
was delivered the following day at 1130 h (approximately 24 h after the
assault occurred). Jurisdiction was assumed by the CMO, and the fetus
and placenta were brought to the CMO for examination.
The fetus was received for postmortem examination encased in
extraplacental membranes. The placenta was separate, and the umbili­
cal cord had been previously clamped and transected. Fetal examination
showed a small for gestational age (SGA) fetus with a mass of 550 g
(511–1195 g expected for 26 weeks, approximately 3rd percentile;
Fig. 1)[1]. External examination showed a structurally normal fetus with
red-brown discoloration of the umbilical stump and mild maceration

* Corresponding author at: Department of Pathology, University of Alabama-Birmingham, 1670 University Blvd, Birmingham, AL 35233, United States.
E-mail address: datherton@uabmc.edu (D.S. Atherton).

https://doi.org/10.1016/j.hpr.2021.300586
Received 30 November 2021; Received in revised form 21 December 2021; Accepted 23 December 2021
Available online 4 January 2022
2772-736X/© 2022 The Authors. Published by Elsevier Inc. This is an open access article under the CC BY-NC-ND license
(http://creativecommons.org/licenses/by-nc-nd/4.0/).
D.S. Atherton et al.
Fig. 1. Fetus at time of examination. The fetus had minimal desquamation/
maceration (less than 5%) of the total body surface area and red-brown
discoloration of the umbilical stump. (For interpretation of the references to
colour in this figure legend, the reader is referred to the web version of
this article.)
with skin desquamation involving less than 5% of the total body surface
area.
Autopsy showed no visible trauma on or within the fetus. Micro­
scopic examination of the heart showed loss of nuclear basophilia in the
inner half of the myocardium and preservation of nuclear basophilia in
the outer half of the myocardium. Features of acute hypoxia/ischemia in
the fetus included small surface petechiae on the lungs and perivascular
hemorrhages in both cerebral hemispheres of the brain. Increased
circulating nucleated red blood cells were present in fetal vessels in the
fetus and in the placenta, a feature supportive of intrauterine hypoxia/
ischemia, although this could be either acute or chronic. Gross and
microscopic examination of several sections of umbilical cord showed
the normal three-vessel arrangement with no stricture, thrombosis,
significant congestion, or necrosis. Examination of the placenta revealed
demise-related involutional changes that included only intravascular
karyorrhexis within villous capillaries, and complete absence of luminal
abnormalities in stem vessels. However, the placenta was low weight for
gestation at 135 g (175–280 g expected for 26 weeks) and showed his­
tologic evidence of chronic ischemia (Fig. 2A). There was no evidence of
abruption. There was no evidence of intrauterine infection in any
placental or fetal tissues.
Based on the history of compression of the mother’s abdomen during
assault, postmortem examination findings that temporally associated
IUFD with the time of the assault, and microscopic findings compatible
with acute hypoxia, the opinion of the cause of death of the fetus in this
Fig. 2. (A) Placenta showing chronic chorionic villous ischemia with focal perivillous fibrinoid (H&E, 4x). The inset (40x) shows villi with increased nucleated red
blood cells and intravascular karyorrhexis. (B) Myocardium showing loss of nuclear basophilia in inner half of myocardium (H&E, 60x). (For interpretation of the
references to colour in this figure legend, the reader is referred to the web version of this article.)
2
Human Pathology Reports 27 (2022) 300586
case was intrauterine fetal demise due to compression of the mother’s
abdomen during an assault. No manner of death was listed as per State
guidelines for fetal deaths.
3. Discussion
Most FPs have little exposure to fetal autopsies during pathology
residency training and even through forensic pathology subspecialty
training. For that reason, fetal autopsies can be challenging. Further­
more, the complex, developing anatomy and sheer number of possible
congenital abnormalities can make postmortem examination of fetuses
intimidating. The purpose of this case report is to highlight the impor­
tance of accurate estimation of time of death in IUFD, particularly for
FPs since it can have legal ramifications.
In October 1992, David Genest, MD, et al. published a three-part
series in Obstetrics and Gynecology entitled “Estimating the Time of
Death in Stillborn Fetuses.”[2–4] They analyzed how well various
postmortem examination features correlated with how long a fetus had
been dead prior to delivery. Specifically, they looked at histological
changes in various fetal organs, histologic changes in the placenta, and
external characteristics of the fetus. Their work has remained the
mainstay for timing of intrauterine fetal demise prior to delivery. They
showed that various degrees and locations of desquamation of the skin
of the fetus, nuclear basophilic changes of various organs, and demise
related involutional changes in the placenta were highly correlated to
post-demise interval (Table 1).
When evaluating the timing of fetal death within the first few days
prior to delivery, features that are particularly useful are assessment of
desquamation/maceration of the fetus and loss of nuclear basophilia in
myocardium. In the present case, maceration was only observed focally
on the left flank and on the back, which was estimated to comprise less
than 5% of the total body surface area (Fig. 3). According to Genest’s
research, these findings (site of desquamation, area of desquamation,
and number of zones of desquamation) correlate with postmortem in­
tervals of the following: ≥12 h, ≥18 h, and ≤ 18 h, respectively. Thus, in
aggregate, these features would suggest a postmortem interval of at least
12 h and up to approximately 18 h.
For myocardium, Genest, et. al., showed that loss of nuclear baso­
philia in the inner half of the myocardium was correlated with a post-
demise interval of ≥ 24 h and loss of nuclear basophilia in the outer
half of the myocardium was correlated with a post-demise interval of ≥
48 h. In our case, examination of several full thickness sections of
myocardium showed loss of nuclear basophilia in the inner half of the
myocardium, but not the outer half of the myocardium (Fig. 2B). Thus,
these histologic findings would suggest that the fetus died between
approximately 24 and 48 h prior to delivery.
For placental histology, Genest, et. al., showed that karyorrhexis of
D.S. Atherton et al. Human Pathology Reports 27 (2022) 300586

Table 1 the intravascular leukocytes and/or endothelial cells in the fetal capil­
Sensitivity, Specificity, and Positive Predictive Value (PPV) of Examination laries of the chorionic villi correlate with a post-demise interval of ≥ 6 h,
Findings as it Relates to Retention Time. and that multifocal (but not extensive) stem villous luminal abnormal­
External Fetal Exam Retention Sensitivity Specificity PPV ities correlate with a post-demise interval of ≥ 48 h. In our case, the
Findings Time findings of intravascular karyorrhexis without stem vessel abnormalities
Desquamation ≥ 1 cm ≥6h 86% 100% 1.00 suggests a demise to delivery interval of 6–48 h.
Desquamation of face, back ≥12 h 80% 100% 1.00 Taking all these findings in aggregate, these examination findings
or abdomen estimate the time of IUFD to be between 24 and 48 h prior to delivery.
Desquamation ≥ 5% of body ≥18 h 80% 100% 1.00
Since delivery occurred at 1130 h on the day after the assault, this es­
Desquamation 2 or more of ≥18 h 90% 92% 0.90
11 zones timates the time of fetal death to be between 1130 h on the day prior to
Mummification ≥2 wks 100% 100% 1.00 the assault and 2330 h on the day of the assault. Ultrasound confirmed
Fetal Organ Histology Retention Sensitivity Specificity PPV IUFD at 1520 h on the day after the assault, so death could not have
Time occurred after that. This creates an approximate 27 h window prior to
Kidney: Loss of tubular 97% 89% 0.97
ultrasound-confirmed death in which death could have occurred, and
≥4h
nuclear basophilia in ≥ 1%
of cells the assault was within this calculated window. This time frame is shown
Liver: Loss of hepatocyte ≥24 h 100% 92% 0.89 in Fig. 4.
nuclear basophilia in ≥ 1% In cases involving a growth restricted fetus and findings of placental
of cells
underperfusion, as in this case, stillbirth is often assumed to have a
Myocardium: Inner half loss ≥24 h 94% 100% 1.00
of nuclear basophilia in ≥ placental cause. However, the correlation in this case between the
1% of cells estimated time of fetal demise and the timing of the assault is suggestive
Myocardium: Outer half loss ≥48 h 100% 96% 0.91 that the two events were related. The assault in this case involved
of nuclear basophilia in ≥ increased pressure on the mother’s abdomen, potentially increasing the
1% of cells
intrauterine pressure enough to overcome fetal and placental compen­
Bronchus: Loss of epithelial ≥96 h 100% 97% 0.91
nuclear basophilia in ≥ 1% satory measures in this presumably already susceptible fetus, with
of cells resulting fatal hypoxia/ischemia of the fetus.
Liver: Loss of nuclear ≥96 h 91% 100% 1.00 Umbilical cord and/or chorionic vascular compression are well-
basophilia in 100% of cells
known etiologies for reduction in blood flow both to and from a fetus.
GI tract: Loss of nuclear ≥1 wk 90% 100% 1.00
basophilia in 100% of cells [5] Umbilical cord compression most commonly occurs as a result of the
Adrenal: Loss of nuclear ≥1 wk 100% 100% 1.00 cord become entangled around a fetus’s neck (a “nuchal” cord), the
basophilia in 100% of cells umbilical cord forming a knot, or from prolapse during uterine con­
Trachea: Loss of chondrocyte ≥1 wk 89% 100% 1.00 tractions during labor and delivery. Chorionic vascular compromise
nuclear basophilia in ≥ 1%
most often occurs in cases of velamentous or marginal cord insertion or
of cells
Kidney: Loss of nuclear ≥4 wks 100% 98% 0.88 in cases of monochorionic twins with amniotic fluid pressure imbalance.
basophilia in 100% of cells If unrecognized and untreated, this reduction in blood flow can lead to
of any type fetal hypoxia, bradycardia, permanent brain damage and even death.
Placental Histology Retention Sensitivity Specificity PPV
[6,7] The exact length of time required to cause permanent brain
Time
Intravascular karyorrhexis ≥6h 94% 100% 1.00
damage or death after reduction or obstruction of fetoplacental blood
Stem vessel luminal flow cannot be certain. In cases of subacute or chronic obstruction to
abnormalities fetal flow, histopathologic changes may be identified, and these were
Multifocal (10–25% of stem ≥48 h 94% 100% 1.00 ruled out in this case. However, in acute obstruction there may be no
villous vessels)
correlative fetal or placental findings in vessels or placenta.
Extensive (greater than 25% ≥2 wks 78% 98% 0.88
of stem villous vessels)
Extensive villous fibrosis ≥2 wks 100% 93% 0.75 4. Conclusion

This case highlights the importance of fetal autopsy findings for

estimation of time of intrauterine fetal demise, particularly in the
context of maternal trauma. It also applies a well-established method of
dating intrauterine fetal death in an atypical setting. Additionally,
consultation with placental and perinatal pathology experts can provide
vital information when assessing the specific histologic findings in these
difficult cases.
This research did not receive any specific grant from funding
agencies in the public, commercial, or not-for-profit sectors.

Patient consent

Patient consent was not available as the case involved fetal remains;
we confirm that no identifying data are included in the manuscript.

CRediT authorship contribution statement

Daniel S. Atherton: Writing – original draft. Brandi C. McCleskey:

Writing – review & editing. Virginia E. Duncan: Writing – review &
Fig. 3. Focal skin desquamation/maceration on back. editing.

3
D.S. Atherton et al.
Fig. 4. A diagram showing a span of three days with the gray portion being the 48 h prior to delivery. Death could not have occurred after the ultrasound (the dotted
line). The assault occurred within the estimated window of fetal death.
Declaration of Competing Interest
The authors declare that they have no known competing financial
interests or personal relationships that could have appeared to influence
the work reported in this paper.
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