© 1996 American Sleep Disorders Association and Sleep Research Society
Apnea in Infants and Children
Rebreathing of Exhaled Gases:
Importance as a Mechanism for
the Causal Association Between Prone Sleep
and Sudden Infant Death Syndrome
James S. Kemp Division of Pulmonary Medicine, St. Louis
Children's Hospital, and Department of Pediatrics, Washington University School of
Medicine, St. Louis, Missouri, U.S.A.
Summary: Twenty to 52% of sudden infant death syndrome (SIDS)
victims are found dead with their noses and mouths turned into underlying bedding. Several
items of bedding have been shown to increase the risk for SIDS in case-control studies or
to be associated with many SIDS deaths in case series. These items of bedding are softer,
limit CO2 dispersal more, and cause more rebreathing of exhaled gases than bedding
infrequently associated with SIDS. Rebreathing of exhaled gases may explain some prone
deaths, and avoiding rebreathing of these gases is one possible mechanism for the
reduction in SIDS when infants avoid prone sleep. Results supporting these statements are
reviewed and discussed. Key Words: Sudden infant death - Rebreathing - Consumer
Some sudden infant death syndrome (SIDS) deaths can be prevented, and avoiding prone
sleeping is the primary reason (1-4). Although the results are pending for the United
States, this first statement is true for many countries in the industrialized world. The
case for this apparent causal association between SIDS and prone sleeping has been
outlined by Mitchell (5). Criteria for causal association (6) included appropriate
temporal sequence, strength of association, specificity of association, and evidence for a
dose effect and for a biologically plausible mechanism. According to Mitchell, the
strongest support for a causal association was the (thus far) consistent finding that SIDS
rates fall when prone sleeping becomes less prevalent.
The purpose of this review is to highlight the epidemiologic and physiologic results
that suggest that rebreathing of exhaled air trapped in bedding is an important potential
mechanism lending biologic plausibility to the association between prone sleeping and
SIDS. Although not essential to establish a causal association, such studies of mechanism
have value when they are based on reliable physiology and on the circumstances of death,
and because they may help us understand some, if not all, aspects of the causal
Prevalence of Face-Down and Face-Into-Bedding Deaths
In terms of rebreathing, the supine, face-up scenario, even when the nose and mouth are
covered by bedding, appears to carry little risk for suffocation (7). Therefore, the
deaths pertinent to rebreathing had occurred face straight down, or nearly so, with the
nose and mouth into bedding, and with the mass of the infant's head acting to force the
nose and mouth into the underlying microenvironment.
Published reports dating back to the 1940s indicate that from 20% to 52% of infants die
suddenly and unexpectedly with nose and mouth down into bedding (8 - 15). In a
case-control series, Carpenter and Shaddick (10) showed that the face-down posture
significantly increased risk of sudden death (p < 0.01). A recent case-comparison study
of 206 deaths in the U.S.A. occurring between 1991 and 1996 showed that 28.6% of SIDS
infants died prone with their airways covered by bedding (15). In summary, review of
published reports reveals the consistent finding that 1/5 to 1/2 of SIDS occurs in a
posture that makes rebreathing possible - face down, with nose and mouth into bedding. For
the U.S.A., the results have been consistently near 30% (8,9,11,14,15).
Four Items of Bedding Related to Prone Face-Down Deaths
Four specific types of bedding will be cited as examples of the potential contribution
of bedding to a dangerous sleep microenvironment. One type was analyzed in a case series,
the others in case-control studies.
Thirty-six deaths occurring on soft pillows or mattresses filled with 3 mm beads of
polystyrene were reported to the U.S.A. Consumer Product Safety Commission. Detailed
review of 25 cases showed that all were prone, and 88% of infants were found dead with
their nose and mouth covered (16).
A case-control study from England (10) showed that being placed to sleep on a soft
pillow significantly increased "cot death" risk in infants (p < 0.01).
Before the intervention phase of the New Zealand Cot Death Study, 41.8% of infants
slept prone, and 64.8% of infants slept on sheepskins. In 71% of SIDS cases there the
infants were "found either face down into a soft mattress or sheepskin or completely
covered by bedclothes"(12). The effect on SIDS risk of sheepskin use has not been
published in detail, but sheepskin use has been reported to increase the odds ratio (OR)
for SIDS in the prone position by as much as two- or three-fold (17).
Mattresses filled with "natural fibers" (including kapok and bark from ti
trees) were identified as "modifiers" increasing the risk of prone SIDS in a
prospective case-control trial from Hobart, Tasmania. The OR for prone sleep, overall, was
4.5 (95% confidence intervals 2.1-9.6); the OR for use of natural fiber bedding,
regardless of sleep position, was only 1.3 (CI=0.6-2.9); however, the OR soared to 10 (CI=
2.5-43) when infants slept prone on natural fiber bedding(18). As was the case,
apparently, with sheepskins, soft bedding used in Tasmania increased the risk for sudden,
unexpected death in prone infants, but the risk was not significant when they were supine.
A related report from Hobart (13) indicated that "39% (of SIDS cases there)... were
found face down in the prone position".
Selected Physiologic Evidence for Rebreathing as a Lethal Mechanism
The studies discussed next were based on personal (14,16) and published observations
(8,10,12,13) that infants are often found dead with noses and mouths turned into bedding.
The physiologic studies were designed to ascertain whether, and how often, this sleep
microenvironment can cause lethal rebreathing of exhaled gases. It is recognized, of
course, that arousal deficits and thermal stress can also contribute to the dangers of the
face-down microenvironment (12,19-22).
Animal Studies of Bedding on Which Infants Died Face Down
A sedated rabbit breathing into items of bedding was used to "physiologically
reconstruct" microenvironments present at death on polystyrene bead-filled cushions
(16), on "ordinary bedding" (14), and on sheepskins (23). The rabbits mounted
vigorous ventilatory responses to the rebreathing challenge (Fig. 1) (22) but,
nevertheless, developed acidemia, progressive hypercarbia, and severe hypoxemia. Profound
abnormalities in gas exchange led to death in four out of four reconstructions on
polystyrene cushions, five out of seven reconstructions on ordinary bedding used by
infants in St. Louis, and three out of four reconstructions on sheepskins.
|FIG. 1 Capnometry tracings from the airway opening of a rabbit.
A. Rabbit breathing fresh air with normal end-tidal CO2 (1% CO2 is
approximately 7mm Hg CO2 at sea level). B. Recording after 5 minutes of
breathing into a sheepskin through the head of a weighed mannequin. Note that the
end-tidal CO2 is near 8% (56mm Hg) and that the inspired CO2 is 5%. Sheepskin has caused
much rebreathing of exhaled gases and impairement in gas exchange despite a vigorous
ventilatory response by the rabbit (used with permission) (23).
Mechanical Model Studies of Bedding and Rebreathing (24,25)
Because bedding on which infants died face down is soft and causes rebreathing in
rabbits and infants(26), mechanical models were developed to better quantify and compare
bedding softness and potential to cause rebreathing of exhaled gases (27,28). Softness was
measured as the area in contact (in cm2) between the face of an
appropriately-weighted infant mannequin head and the underlying bedding. Potential to
cause rebreathing of exhaled gases was measured (27) as the half-time (t1/2)
for disappearance of CO2 from a microenvironment made up of the item of bedding
and the face-down mannequin head ventilated with a syringe containing 5% CO2.
Firm beds with minimal covering had smaller areas of contact and shorter t1/2
times. Bedding associated with face-down SIDS (including sheepskins, ti tree mattresses,
etc.) was softer and had longer t1/2 times (Fig. 2) (28).
|FIG. 2 Comparison of physical properties of bedding associated
with face-down SIDS to those with presumably safe bedding. Open bars from firm mattresses
covered with a sheet. Bedding associated with face-down SIDS (shaded bars) is softer and
has a greater potential to limit CO2 dispersal than does bedding on wich
face-down deaths are rare (used with permission) (28).
It is apparent that items of bedding associated with SIDS, whether unusual or ordinary,
share important physical properties that favor rebreathing of exhaled air (28).
It should be emphasized that neither the rabbit nor the mechanical reconstructions are
models of closed systems with finite quantities of O2 available. Rather, it was
assumed that the weighted head on soft bedding created a partial seal about the face. This
assumption is based on the pattern of arterial blood gas changes seen in the rabbit
studies (14,16,23). Futhermore, one unexplored aspect of these microenviroments is the
possibility that some bedding constituents (e.g. polystyrene, wool) might retain CO2
preferentially near the infant's external airway when face down.
Summary and Conclusions
The above is a selection of epidemiologic and physiologic evidence for rebreathing of
exhaled gases as an important lethal mechanism when prone infants die face down. It is
pertinent in the 20 - 52% of all sudden deaths that occur this way. Furthermore, it has
been our repeated observation that when the mannequin head is covered when face up that
there is little abnormality in gas exchange in the rabbit model and only slight
prolongation on the rate of CO2 dispersal from the mechanical model. Thus, even
when covered by the type of bedding and the number of layers of bedding used by infants in
the U.S.A., the risk for rebreathing of exhaled gases for a supine infant seems low.
Certainly, if the face is completely uncovered, the risk of rebreathing exhaled gases is
nil. These analyses suggest that rebreathing of exhaled gases offers a biologic mechanism
for some prone deaths that is circumvented when infants are supine. In other words,
rebreathing of exhaled gases can explain many prone deaths and avoiding rebreathing of
exhaled gases can explain, in part, why there is less SIDS when infants are non-prone.
Acknowledgements: This work was supported by a research grant
from the American Lung Association and by a grant from the Sudden Infant Death Syndrome
Accepted for publication September 1996.
Address correspndence and reprint requests to:
James S. Kemp M.D.
St. Louis Children's Hospital
1 Children's Place
St. Louis, MO 63110, U.S.A.
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