PEDIATRICS Vol. 107 No. 4 April 2001, pp. 693-698

Thermal Stress in Sudden Infant Death: Is There an Ambiguity With the Rebreathing Hypothesis?

Warren G. Guntheroth, MD and Philip S. Spiers, PhD

From the Department of Pediatrics, University of Washington School of Medicine, Seattle, Washington.

	ABSTRACT

Top Abstract References

Objective.  To assess the role of thermal stress in the cause of sudden infant death syndrome (SIDS), and to compare risk factors with those of rebreathing.

Methodology.  Analysis of publications concerning the epidemiology and physiology of thermal stress in SIDS.

Results.  A strong association between thermal regulation and ventilatory control was found, specifically for prolonged apnea. Infections, excessive room heat and insulation, and prone sleeping produce significantly increased odds ratios for SIDS. Although some of the risk factors for rebreathing could be explained by the effects of thermal stress, several factors for thermal stress could not reasonably be explained by the rebreathing hypothesis.

Conclusions.  Although the risk of thermal stress is widely accepted abroad, it has received relatively little attention in the United States. The incidence of SIDS in the United States can likely be further reduced by educating the public against the dangers of overheating, as an integral part of the back-to-sleep campaign.  Key words:  sudden infant death, thermal stress, rebreathing suffocation.

Thermal stress and moderate hyperthermia (fever) have been implicated in sudden infant death syndrome (SIDS) since 1980, when Stanton and colleagues¹ suggested that an interaction between fever and excessive bedclothes was responsible for a form of heat stroke. Since then, thermal stress and SIDS have been linked with increasing frequency in England, Europe, Australia, and New Zealand, but little concerning this subject has appeared in the medical literature of North America until the American Academy of Pediatrics' recent position paper² on amenable risk factors. And yet, thermal stress is a risk that is as amenable to intervention as that associated with prone sleeping.³

	THERMAL REGULATION

Thermal stress describes a condition that is a threat to the organism's thermal regulation, but may be mild enough to permit core temperature to remain within normal limits. Hyperthermia has been used as a term equivalent to thermal stress, but hyperthermia should be reserved for conditions in which the core body temperature is elevated, such as with fevers. Severe hyperthermia may be attributable to specific entities, such as malignant hyperpyrexia, that cause relatively specific changes in small bowel mucosa⁴ and should be distinguished from SIDS by definition.⁵

For homeotherms, temperature regulation involves a balance between endogenous heat production and heat loss. Heat production depends on the metabolism of the infant, including muscular activity (conscious, rapid eye movement sleep, and shivering), nonshivering thermogenesis, and fever. Heat loss is determined by the ambient temperature, radiation to and from heat sources (including adults in close proximity), convection, insulation (total and partial, particularly of the head and belly), sweating, and vasoconstriction. Obviously, >1 factor can operate at the same time, potentially causing a cumulative lethal effect.

	RISK FACTORS FOR SIDS ATTRIBUTABLE TO THERMAL STRESS

Infection

The idea that apparently mild infections, a characterization based on the severity of anatomic changes at autopsy, could cause sudden death was put forth in 1938 by Goldbloom and Wigglesworth.⁶ Werne and Garrow⁷ added to the evidence for the role of infection and refuted the role of suffocation by bedclothes, a theory that had become popular in the 1940s.⁸ Adelson and Kinney in 1956⁹ found mild inflammatory changes at autopsy in 84% of their cases of SIDS.

In 1984, Stanton¹⁰ retracted his earlier hypothesis that heat stroke was the lethal aspect of hyperthermia, and suggested that moderate hyperthermia had led to prolonged apnea as the mechanism leading to cot death. Febrile illnesses were present in 17 of his 34 victims. He reported subsequent success in preventing prolonged apnea in infants admitted for near-miss cot deaths by educating their mothers against overheating and overdressing the infant, particularly in the presence of infections.

Epidemiologic data on the role of infections were reported from the National Institute of Child Health and Development epidemiologic study¹¹; they recorded histories of upper respiratory infections significantly (P < .01) more often among white SIDS victims than among controls. From the same study, diarrhea and vomiting within 2 weeks of death were reported significantly (P < .001) more often in SIDS victims.¹²

Prolonged sleep apnea in association with infections was reported by several investigators,^13-16 but the role of hyperthermia as an intermediary between infection and apnea or SIDS was not suggested until Stanton's 1984 report.¹⁰

Nelson et al¹⁷ returned to the combination indicted by Stanton (fever secondary to infection and excessive clothing) and added prone sleeping as a major risk for thermal stress and SIDS. Their modeling of thermal balance predicted that prone sleeping would interfere with normal heat loss by reducing the surface of the face exposed for heat loss.

In 1992, Gilbert et al¹⁸ showed that the risk of infection was greatest when the infant was overwrapped; the combination produced an astounding odds ratio (OR) for SIDS of 51.5 (95% confidence interval [CI]: 5.64-471). But infection does not have to produce overt fever to produce thermal stress. Jackson et al,¹⁹ using long-term recordings of rectal temperatures in normal infants, found that the infant's temperature rose to the upper limit of normal 3 days before any other signs of an illness.

Infections have been invoked as an explanation for the higher rate of SIDS in the winter and there is a consensus that infections are more common then, perhaps because school is in session; older children are likely to bring home a virus contracted at school to infant siblings.²⁰ A tendency of parents to use more bedclothing if the infant has an infection increases the risk of thermal stress and SIDS,²¹ consistent with Stanton's anecdotal observations.¹⁰

Interleukins have been suggested as a humoral link among infection, thermal stress, somnolence, and sleep apnea.^22-24 Fleming²⁵ accepted these mediators as a link to peripheral vasoconstriction and increased metabolism in brown adipose tissue as a result of acute infections, and proposed that the effects of thermoregulation on respiratory control could give rise to prolonged apnea.

Although Naeye²⁶ regarded persistence of periadrenal brown fat in SIDS victims as evidence of previous episodes of hypoxia, the chief function of brown fat is probably nonshivering thermogenesis, and its abnormal persistence could also be interpreted as evidence of repeated infections with fever. This interpretation is consistent with the increased  globulin levels in SIDS victims found by Valdes-Dapena,²⁷ and with increased T3 levels reported by Chacone and Tildon.²⁸

Climatic and Room Temperature

Thermal stress from warm weather is not a problem as long as the infant is allowed to sweat and there is no impediment to evaporation. In fact, SIDS is much less common in the summer.²⁰

It may seem counterintuitive to a theory of thermal stress that there is an inverse relation between the mean climatic temperature and the incidence of SIDS, but this relationship was established by Ponsonby et al.²⁹ One explanation is that parents decide on the infant's bedroom temperature in winter based on their perception of the cold weather. Fleming et al³⁰ found that leaving the heat on all night in the infant's room created a relative risk of 2.7 (CI: 1.4-5.2; P < .01). Similarly, any bedroom heating during the SIDS victim's last sleep was found to be a predictor (P = .039) of SIDS.³¹ Tufnell and colleagues,³² from 1197 overnight recordings in infants, found that rectal temperature was directly related to increased room temperature.

Two early studies^33,34 found that premature infants developed more frequent apnea at warmer ambient temperatures (90°F). In 1983, Steinschneider³⁵ published his laboratory protocol in which he used this ambient temperature to increase the frequency and duration of apneic episodes during naps, although he did not refer to thermal stress as a risk factor for SIDS.

The preceding reports involve a subtle form of thermal stress without hyperthermia. However, inadvertent death of a helpless infant by true hyperthermia has been documented. Bass³⁶ reported on twins who succumbed to the effects of a room temperature of 39°C; the victims were warmly dressed and covered with 2 blankets.

Excessive Insulation of the Infant

Excessive bedclothes on infants are an ancient problem according to Bacon.⁴ He quoted Cadogan, who wrote in 1748, "The first great Mistake is that they (mothers) think a new-born Infant cannot be kept too warm; from this Prejudice they load it and bind it with Flannels, Wrappers, Swathes, Stays, etc.". The practice of swaddling has by no means disappeared. Ponsonby and coworkers³⁷ found that swaddling at the time of death was a risk factor for SIDS, but only in the prone position, with an OR of 8.9 (CI: 2.4-34).

As with room heating, excessive bedclothes may play a significant role in the seasonality of SIDS because parents apparently decide on how to dress the infant based on the outdoor temperature, rather than the temperature in the infant's room.³⁸

Affluence may have a risk in terms of bedclothing: in Holland an increasing trend toward the use of down in infant sleepwear, which, along with central heating, increased the chances of overheating and SIDS. However, after adjustments for confounders,³⁹ the effect of the duvet was not significant, a conclusion also reached in New Zealand by Mitchell et al.⁴⁰ But, when the down comforter covered the head, l'Hoir and colleagues³⁹ found a very high OR of 38.02 (CI: 3.20-452).

Fleming and his group³⁰ were the first to quantify the risk of excessive bedding in relation to SIDS. They concluded that overdressing combined with the prone position was associated with a relative risk to SIDS of 15 to 25, depending on the age.

A similar effect was observed in New Zealand.⁴¹ An interaction between sleeping prone and insulation >2 tog (a unit of thermal resistance with specified heat flow) was associated with an OR for SIDS of 6.07 (CI: 3.83-9.60).

It may seem unlikely that the heat production of an infant insulated by simple blankets could result in fatal hyperthermia, but Jardine and Haschke⁴² convincingly demonstrated this outcome using piglets.

Head Covered With Bedding

The brain accounts for 40% of the total oxygen consumption in infants, and produces roughly that proportion of body heat.⁴³ When the infant is heavily wrapped in blankets and in the prone position, 85% of the total heat loss is through the face and head.^17,30 Fleming and colleagues⁴⁴ found that the OR for SIDS when the head was covered was 21.6 (CI: 6.2-75.0), which they attributed to thermal stress.

Another animal model using newborn piglets sleeping under thick bedding⁴⁵ showed that covering the head for 2 hours caused a rapid rise in body temperature but no change in arterial O₂ and the CO₂ actually fell. This group⁴⁶ subsequently examined the pathophysiology of animals that were kept covered until death; they observed hyperthermia, hypoxia, metabolic acidosis, and respiratory alkalosis, and finally, apnea.

In human infants, covering the head with only a single blanket was used to look at the alternate possibility of respiratory acidosis attributable to rebreathing. In 22 normal infants, Malcolm and coworkers⁴⁷ found that covering the infant's head caused a rapid increase in CO₂ around the mouth within 1 or 2 minutes, but the infants then settled into a steady state with no tendency for additional increases of CO₂. By monitoring oxygen saturation, they found that no infant developed hypoxia. They concluded that their results did not support the rebreathing suffocation hypothesis. (They also observed that the use of a pacifier under the blanket promoted a rise in inspired CO₂ whether prone or supine; pacifiers have been shown to have a protective effect against SIDS⁴⁸).

Additional centers have reported significant risks associated with covering the head with bedding, particularly when the infant was sleeping prone.^39,49 The first report, from the Netherlands, attributed death to thermal stress, and the second, from Germany, listed several possibilities, beginning with thermal stress but including rebreathing.

A 1996 report from Kleemann's group⁵⁰ described profuse sweating associated with the head being covered by bedding. Skadberg and Markestad⁵¹ obtained results similar to Malcolm's; in the prone position, infants developed a rise in skin temperature, and a rise in transcutaneous PO₂. They concluded, "normal infants are able to eliminate CO₂ immediately."

Soft Bedding

Carpenter and Shaddick⁵² were the first to report that soft mattresses and the use of pillows were associated with cot death (P = .01).

In an Australian study, mattresses filled with kapok or bark were found to have no effect on the rate of SIDS, but when analyzed for prone sleepers only, there was a significant interaction that increased the risk associated with the prone position.³⁷ Natural fiber mattresses are quite malleable and therefore increase the surface area of the infant in contact with the insulating effect of the mattress. Ponsonby and colleagues³⁷ listed both asphyxiation and hyperthermia as possible mechanisms for the risk of prone sleeping on soft mattresses. Of the other 3 risk factors that significantly interacted with prone sleeping, swaddling could also be attributed to either rebreathing or thermal stress, but a recent illness and heat in the infant's bedroom relate only to thermal stress.

Sleeping on sheepskin has been suggested to increase the risk of SIDS through rebreathing suffocation. However, Ponsonby and coworkers in Tasmania³⁷ found a slightly lower (but not significant) risk of SIDS when sleeping occurred on sheepskin, and no additive or multiplicative interaction with prone sleeping. In New Zealand,⁵³ 42% of both controls and SIDS victims used sheepskin (no significant effect), but if only infants sleeping prone were studied, a significant interaction was found representing an increased risk for SIDS in the use of sheepskin (adjusted OR 1.70; CI: 1.08-2.67). These authors concluded that the risk of sleeping on sheepskin is consistent with either rebreathing or thermal stress.

Mitchell's group⁵⁴ reported that sleeping on soft mattresses increased the risk of SIDS, with an adjusted OR of 2.36 (CI: 1.06-5.25), but the degree of firmness did not interact with the sleep position of the infant. If a soft mattress caused rebreathing as the mechanism of death, the risk should apply only while in the prone sleep position, whereas a reduction of the skin surface for heat loss would presumably increase the risk of SIDS in any sleep position.

Prone Sleeping

Prone sleeping is the single most potent risk factor for SIDS^30,55,56 and has proven to be the most modifiable risk factor. As early as 1989,^17,30 thermal stress was implicated in this risk.

The risk to thermal balance of prone sleeping is twofold. The ventral surface of the infant allows greater heat loss than the dorsal surface, and the headparticularly the faceis the major source of heat loss when the infant is under thick clothing or bedding.^17,25 Bolton and colleagues⁵⁷ quantified the effects of heat loss from the body, and calculated the highest tolerable ambient temperature for a given set of clothes and bedding. A well-wrapped infant lying face down could tolerate an ambient temperature of 10°C less than if it were lying supine. Tuffnell et al⁵⁸ calculated that heat loss in prone infants was 60% less than for nonprone sleeping infants, with the same insulation values for clothing and bedding.

Mitchell⁵⁹ listed the significant modifiers of the risk of prone sleeping, namely season, latitude, illness, thermal insulation, and sheepskin. His opinion was that the mechanism by which prone sleeping position causes SIDS involves the infant's thermal balance.

Bedsharing

Cosleeping has been advocated as more natural for the child and mother,⁶⁰ but it involves a definite risk for SIDS, particularly if the parents smoke. Mitchell and colleagues⁶¹ found that the risk of bedsharing increased in the summer and concluded that thermal stress caused the increase. Studies have shown that the infant frequently has its head covered when sleeping in the mother's bed, and the total insulation is increased for the infant, not to mention the heat source provided by the mother's body under shared blankets.^62,63

Sweating

A history of profuse sweating ("drenching night sweats") was reported by Beal in 1983⁶⁴ in 48% of 160 SIDS victims. This is compatible with hyperthermia or at least thermal stress, although Beal reported no relationship to the weather or to bedclothes. Kahn⁶⁵ found that profuse sweating was 1 of the 2 most significant predictors of SIDS in Brussels; he and his colleagues postulated that this phenomenon represented an abnormality of function of the autonomic nervous system.

Kleemann and coworkers⁵⁰ found that sweaty clothing and bedding was associated with SIDS with an OR of 17.9 (CI: 8.7-37.1), and concluded that hyperthermia was the mechanism because sweating was associated with finding the victim's head under the bedding (P < .001). A New Zealand study found that drenching night sweats at least once weekly were reported in 15.6% of SIDS cases, compared with only 5.9% of control infants.⁶⁶

Passive Smoking

The postnatal effects of parental smoking on their infant presumably include the well-established vasoconstrictive effects of nicotine, which has the effect of decreasing blood flow to the skin, and thereby decreasing heat loss. Vasoconstriction would increase rectal temperatures; the latter has been documented in infants whose parents smoked.³²

Ambiguity of Risk Factors for Thermal Stress With the Rebreathing Hypothesis

Many of the risk factors for thermal stress have also been listed as risk factors for rebreathing suffocation^67-69 (Table 1). Kemp and Thach,⁶⁷ in support of their epidemiologic data, devised an experimental model to support their rebreathing hypothesis. We⁷⁰ have previously expressed reservations about these epidemiologic and animal studies, but here we want to examine whether the individual risk factors for thermal stress could explain SIDS as well or better than the risk factors listed for the rebreathing hypothesis.

Rebreathing has been evoked to explain the danger of prone sleeping when the infant's face is toward a surface of the mattress or pillow that is semipermeable to gases. The hypothesis predicts that carbon dioxide accumulates in the inner volume of the bedding and oxygen gradually diminishes as the experimental animal rebreathes this gas, ending in death.^67-69 Alternatively, as detailed above, there are epidemiologic studies and animal experiments that conclude that prone sleeping increases the risk of SIDS acting through thermal stress.^{17,30,44,57-59,61} Similarly, sleeping with the head covered has been considered a risk for SIDS through rebreathing,^49,52,67-70 but has also been attributed to thermal stress.^{17,39,44-47,49-51}

As seen in Table 1, additional risk factors of soft mattresses and pillows, sleeping on sheepskin, bedsharing, and sleeping in swaddling clothes in the prone position have all been claimed to be risk factors through rebreathing and thermal stress.

However, there are at least 6 additional risk factors for thermal stress that provide no logical support for rebreathing as a mechanism of their lethal effect, namely excessive sweating, excessive room temperature, infection with fever, the seasonal distribution of SIDS deaths, excessive bedclothes, and passive cigarette smoking. Nevertheless, it is possible that both thermal stress and rebreathing are interrelated cofactors of a lethal process that could lead to SIDS through failure to arouse or respiratory failure. Defects in brainstem function from earlier injuries could increase the susceptibility to either mechanism.

From a review of animal, clinical, and epidemiologic studies it was our conclusion that rebreathing suffocation could not easily explain more than a rare death in a seriously impaired infant.⁷⁰ By contrast, from a review of the evidence from around the world on the role of thermal stress in SIDS, we conclude that deaths attributed to rebreathing could more logically be attributed to thermal stress. Still, in a preventive program against SIDS, both thermal stress and rebreathing should have as common objectives the avoidance of prone sleeping, soft bedding, and covering the head. It must be stressed, however, that there are risks of thermal stress that are not covered in the warnings relating to rebreathing suffocation.

A vigorous public campaign warning of heat stress as a preventable risk factor should further reduce the risk of infants to SIDS, and would help focus on the major objective of the back-to-sleep campaign, namely, the supine sleeping position for infants.

	FOOTNOTES

Received for publication May 9, 2000; accepted Aug 3, 2000.

Address correspondence to Warren G. Guntheroth, MD, Box 356320, University of Washington, Seattle, WA 98195-6320. E-mail: wgg{at}u.washington.edu

	ABBREVIATIONS

SIDS, sudden infant death syndrome; OR, odds ratio; CI, confidence interval.

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