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In Depth
Maceration and the Timing of Intrauterine Death
Richard M. Pauli, M.D., Ph.D.
Maceration is the process of tissue degeneration which begins to occur as soon
as an undelivered infant dies. It arises secondary to the effects of autolytic
enzymes. Since this process occurs in what is usually a sterile environment, the
changes which arise are unlike those which occur following other deaths.
There are multiple reasons for trying to estimate the time of fetal death. Such
information is of some importance to a babys parents; in fact, nearly all parents
desire to know when their baby died. Certainly differentiation of intrapartum
andprepartum deaths is relevant to the assessment of any methods of
intervention or prevention; intrapartum deaths are less often of fetal origin and
may include instances more amenable to medical intervention. Estimation of
timing of death also may help in assessing whether a proposed cause of death isreasonable.
Only occasionally, however, is independent documentation of the time of fetal
death obtained. For example, it is uncommon to have ultrasonographic
evaluations close enough together to bracket the time of death accurately. Most
often, then, assessing severity of maceration is the only method available for
confirming when death occurred.
The sequence of macerative changes has been well described. Within hours
after death changes occur in the epidermal-dermal junction resulting in what
usually is termed skin slippage. If the skin is rubbed the epidermis will detach
from the underlying tissues. Shortly thereafter, fluid begins to accumulate under
the skin. Bullae (blisters) may develop (which should not be misinterpreted as
being secondary to an abnormality of development such as epidermolysis
bullosa). These bullae rupture spontaneously or from delivery resulting in
patchy denudation of the skin. Sloughing of skin from larger and greater
number of surfaces indicates that the interval between death and delivery is
longer. With antenatal death more than a few days prior to delivery other
changes begin to occur including generalized hypermobility of joints, change inthe color of the fetal skin surfaces to a pale grey-yellow and liquefaction of
internal organs.
Qualitative scales can be generated based upon this sequence of events. We
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chose to use a five-grade scale based primarily on the external characteristics
of the stillborn, since virtually all infants with studies submitted to WiSSP are
clinically assessed and since we usually could double check the estimates of
maceration using submitted photographs. That scale of severity of maceration is
as follows:
None
Slight -- skin slippage, rare bullae, little (e.g. scrotum only or single spots of
skin loss elsewhere) or no denudation
Mild -- focal denudation of multiple regions without other changes
Moderate-- generalized skin maceration/ denudation but without significant
compressive changes Advanced -- compression and/or mummification and/or
internal liquefaction
Examples of each of these are shown in the figures.
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In the WiSSP series, the distribution of degree of maceration in the first 1040stillborns is:
None 16.0%
Slight 11.6%
Mild 17.7%
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Moderate 29.4%
Advanced 22.5%
(with the rest "indeterminate").
Note that intrapartum deaths (babies with no macerative changes) are quite
infrequent, accounting for only about a sixth of all stillborns.
Given the relevance of severity of maceration to timing of fetal death, it is a little
surprising that no careful assessment of the absolute relationship (rather than
just the sequence) between macerative changes and interval since death was
attempted until recently. Prior to then we could only vaguely correlate severity
of maceration and interval since death. A series of articles (References 1-3)
appeared in 1992 which made such estimation much more precise. David
Genest and his colleagues conducted careful assessments of fetuses in whom
timing of death was well documented. From those assessments they were able
to provide far more specific information about the absolute timing of externalmacerative changes, internal histologic changes and placental changes. Related
to external characteristics they found that changes occurred somewhat more
rapidly than previously assumed. Six of their measures seem applicable to the
scale used by WiSSP:
FeatureInterval between death and
delivery
Skin desquamation of > or =1 cm > or = 6 hours
Skin desquamation involving the face, back
and/or abdomen> or =12 hours
Skin desquamation involving at least 5% of
body surface> or = 18 hours
Change of skin coloration to tan or brown > or = 24 hours
Generalized skin desquamation > or = 24 hours
Mummification > or = 14 days
Note that Genest failed to find any good measures for intervals between 24
hours and 2 weeks. Nonetheless, based on these findings we can better
estimate the relationship between our maceration scale and time interval
between death and delivery:
None = intrapartum death
Slight = less than 12 hours between death and delivery
Mild = about 12-24 hours between death and delivery
Moderate = one to a few days between death and delivery
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Advanced = more than a few days between death and delivery.
The gap between 24 hours and 2 weeks can be filled using histologic features if
they are adequately searched for. Genest et al. found that the distribution of a
single feature on routine histologic slides allowed for interval estimates. That
feature was loss of nuclear basophilia (loss of hematoxylin staining of
nucleoproteins of cells) of a particular organ:
Loss of at least 1% of nuclear staining -
Kidney tubules > or = 4 hours
Hepatocytes > or = 24 hours
Inner half of Myocardium > or = 24 hours
Outer half of Myocardium > or = 48 hours
Bronchial epithelium > or = 96 hours
Loss of all or virtually all nuclear staining -
Liver > or = 96 hours
GI tract > or = 1 week
Adrenal > or = 1 week
Tracheal chondrocytes > or = 1 week
Kidney > or = 4 weeks
We have not routinely included estimates of time interval between death and
delivery in our summaries. We would be interested in knowing whether
inclusion of such an estimate would be helpful to referring health care providers.
Further Reading*
1. Genest DR, Williams MA, Greene MF: Estimating the time of death in
stillborn fetuses: I. Histologic evaluation of fetal organs; and autopsy study of150 stillborns. Obstet Gynecol 80:575-584, 1992.
2. Genest DR: Estimating the time of death in stillborn fetuses: II. Histologic
evaluation of the placenta; a study of 71 stillborns. Obstet Gynecol 80:585-
592, 1992.
3. Genest DR, Singer DB: Estimating the time of death in stillborn fetuses: III.
External fetal examination; a study of 86 stillborns. Obstet Gynecol 80:593-
600, 1992.
4. Wigglesworth JS: The macerated stillborn fetus, in Perinatal Pathology,
Philadelphia: Saunders, 1984, pp. 84-92.
*Copies of these and other relevant articles are available for personal use by
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request from WiSSP.
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