Sleep, 19(10):S263-S266
© 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 product safety.

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 association.

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.

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 (t_1/2) 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 t_1/2 times. Bedding associated with face-down SIDS (including sheepskins, ti tree mattresses, etc.) was softer and had longer t_1/2 times (Fig. 2) (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 Alliance.

Accepted for publication September 1996.
Address correspndence and reprint requests to:
James S. Kemp M.D.
Pulmonary Medicine
St. Louis Children's Hospital
1 Children's Place
St. Louis, MO 63110, U.S.A.

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