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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 baby’s parents; in fact, nearly all parents desire to know when their baby died. Certainly differentiation of intrapartum and prepartum 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 is reasonable.

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 in the 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 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.

 

In the WiSSP series, the distribution of degree of maceration in the first 1040 stillborns is:

None 16.0%
Slight 11.6%
Mild 17.7%
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 external macerative 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:

Feature Interval 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

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 of 150 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 request from WiSSP.

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