Evolution and the sudden infant death syndrome (SIDS)

This paper extends the evolutionary and developmental research model for SIDS presented in previous articles (McKenna 1990a, 1990b). Data from variety of fields were used to show why we should expect human infants to be physiologically responsive in a beneficial way to parental contact, one form of which is parent-infant co-sleeping. It was suggested that on-going sensory exchanges (touch, movement, smell, temperature, etc.) between co-sleeping parent-infant pairs might diminish the chances of an infantile cardiac-respiratory crisis (such as those suspected to occur in some SIDS cases). In this article we review recent epidemiological data and sleep research findings on SIDS to show how they relate to evolutionary and cross-cultural perspectives. Results of a preliminary study of the co-sleeping behavior of mother-infant pairs indicate that, with respect to sleep, arousal, and respiratory patterns, co-sleeping mother-infant pairs affect each other in potentially important ways. We suggest specifically that co-sleeping may shorten periods of consolidated sleep among young infants by causing them to arouse more frequently. Moreover, we suggest that partner-induced arousals might help the infant to confront sleep crises more competently. In the long run, these arousals might prevent the premature emergence of prolonged (adultlike) sleep bouts from which some infants have difficulty arousing—especially during a breathing pause or apnea.     

Sleep and arousal patterns of co-sleeping human mother/infant pairs: a preliminary physiological study with implications for the study of sudden infant death syndrome (SIDS)

The prevailing research design for studying infant sleep erroneously assumes the species-wide normalcy of solitary nocturnal sleep rather than a social sleeping environment. In fact, current clinical perspectives on infant sleep, which are based exclusively on studies of solitary sleeping infants, may partly reflect culturally induced rather than species-typical infant sleep patterns which can only be gleaned, we contend here, from infants sleeping with their parents--the context within which, and for well over 4 million years, the hominid infant's sleep, breathing, and arousal patterns evolved. Our physiological study of five co-sleeping mother-infant pairs in a sleep lab is the first study of its kind to document the unfolding sleep patterns of mothers and infants sleeping in physical contact. Our data show that co-sleeping mothers and infants exhibit synchronous arousals, which, because of the suspected relationship between arousal and breathing stability in infants, have important implications for how we study environmental factors possibly related to some forms of the sudden infant death syndrome (SIDS). While our data show that co-sleeping mothers and infants also experience many moments of physiological independence from each other, it is clear that the temporal unfolding of particular sleep stages and awake periods of the mother and infant become entwined and that on a minute-to-minute basis, throughout the night, much sensory communication is occurring between them. Our research acknowledges the human infant's evolutionary past and considers the implications that nocturnal separation (a historically novel and alien experience for them) has for maternal and infant well-being in general and SIDS research strategies in particular.     

Evolution and the sudden infant death syndrome (SIDS)

Postnatal parent-infant physiological regulatory effects described in the previous paper (Part I) are viewed here as being biologically contiguous with events that occur prenatally, preparing and sensitizing the fetus to the average microenvironment into which the infant is expected, based on its evolutionary past, to be born. Following McKenna (1986), evidence (some of which is circumstantial) is presented concerning fetal hearing and fetal amniotic liquid breathing as they are affected both by maternal cardiovascular blood flow sounds in the uterus and by fluctuating maternal blood sugar levels. These data are linked in turn to the infant’s postulated postnatal responsivity to parental sensory cues, including auditory and vestibular respiratory cues that may assist infants as they “learn” to breathe and, for some, to resist a SIDS event. Data on the respiratory and vocalizing behavior of normal and hearing-impaired persons are used to show that not all forms of human breathing are innate; some forms develop with experience. These data reveal how human infants learn, for example, to coordinate higher and lower brain respiratory nuclei in the context of learning initially to cry with intent and purpose and later to speak. Voluntary, cortex-based breathing emerges at the same time that infants are most likely to die from SIDS, between 2 and 4 months of age. This switch between voluntary and involuntary breathing during both sleep (while dreaming) and wake cycles, which depends on the integration of higher cortical and lower brain stem nuclei, is complex and is possibly the basis of the human species’ unique susceptibility to SIDS—a syndrome as yet unrecognized in other species. These human infant vulnerabilities, including delayed maturity, can explain in part why natural selection ought to favor increased infant sensitivity to parental sensory cues provided by a caregiver—stimuli available in the evolving parental care environment that included parent-infant co-sleeping for more than 4–5 million years of human evolution.     

Bed-Sharing in the Absence of Hazardous Circumstances: Is There a Risk of Sudden Infant Death Syndrome? An Analysis from Two Case-Control Studies Conducted in the UK

Objective

The risk of sudden infant death syndrome (SIDS) among infants who co-sleep in the absence of hazardous circumstances is unclear and needs to be quantified.

Design

Combined individual-analysis of two population-based case-control studies of SIDS infants and controls comparable for age and time of last sleep.

Setting

Parents of 400 SIDS infants and 1386 controls provided information from five English health regions between 1993–6 (population: 17.7 million) and one of these regions between 2003–6 (population:4.9 million).

Results

Over a third of SIDS infants (36%) were found co-sleeping with an adult at the time of death compared to 15% of control infants after the reference sleep (multivariate OR = 3.9 [95% CI: 2.7–5.6]). The multivariable risk associated with co-sleeping on a sofa (OR = 18.3 [95% CI: 7.1–47.4]) or next to a parent who drank more than two units of alcohol (OR = 18.3 [95% CI: 7.7–43.5]) was very high and significant for infants of all ages. The risk associated with co-sleeping next to someone who smoked was significant for infants under 3 months old (OR = 8.9 [95% CI: 5.3–15.1]) but not for older infants (OR = 1.4 [95% CI: 0.7–2.8]). The multivariable risk associated with bed-sharing in the absence of these hazards was not significant overall (OR = 1.1 [95% CI: 0.6–2.0]), for infants less than 3 months old (OR = 1.6 [95% CI: 0.96–2.7]), and was in the direction of protection for older infants (OR = 0.1 [95% CI: 0.01–0.5]). Dummy use was associated with a lower risk of SIDS only among co-sleepers and prone sleeping was a higher risk only among infants sleeping alone.

Conclusion

These findings support a public health strategy that underlines specific hazardous co-sleeping environments parents should avoid. Sofa-sharing is not a safe alternative to bed-sharing and bed-sharing should be avoided if parents consume alcohol, smoke or take drugs or if the infant is pre-term.     

Maternal proximity and infant CO2 environment during bedsharing and possible implications for SIDS research

Sudden infant death syndrome (SIDS) is the leading cause of human infant mortality after the neonatal period in Western countries. Recently, child care practices have been shown to be important in determining infant vulnerability to SIDS. However, very little is known about the impact of parent-infant cosleeping on infant sleep physiology and behavior and SIDS risk. This reflects the failure of Western societal research paradigms to appreciate the human infant's evolutionary history of cosleeping, the recency of the emergence of solitary infant sleeping as a practice and the fact that parent-infant cosleeping is still the preferred sleeping arrangement for the majority of contemporary societies. Incorporating current hypotheses on the mechanisms of SIDS, we have hypothesized that the comparatively sensory-rich cosleeping environment might be protective against SIDS in some contexts. As a first step to characterize cosleeping environments, this investigation is aimed at assessing, in routinely bedsharing mothers and infants, their relative sleeping positions and the potential for sleeping in close face-to-face proximity and for infant exposure to increased environmental CO2 produced by maternal respiration. The latter is important in that breathing elevated levels of CO2 can have diverse effects, ranging from respiratory stimulation at low levels to suffocation at very high levels. Two related laboratory studies were performed. In the first, all-night videotapes of 12 healthy, routinely bedsharing mother-infant pairs were analyzed for sleeping positions and time spent in face-to-face orientation and distances separating their faces. Infants were 11–15 wk old. Mothers predominantly positioned themselves on their sides facing their infants, with the infants placed either supine or on their sides. Mothers and infants slept oriented face-to-face for 64 ± 27% (S.D.) of non-movement time, with distances less than 20 cm commonly separating their faces. In the second study, concentrations of CO2 in air were measured in six young women at distances of up to 21 cm from their nares. Peak expiratory CO2 concentrations remained above 1.0% at distances up to 9 cm and above 0.5% at 18 cm. Both baseline and peak CO2 levels were further increased at all distances when measured within a partial air pocket created to simulate a bedding environment sometimes seen during bedsharing. We conclude that during bedsharing there is potential for 1) a high degree of face-to-face orientation and close proximity and consequently 2) increased environmental CO2, as a result of maternal respiration, to non-lethal levels that might stimulate infant respiration. The close proximity would also maximize the sensory impact of the mother on the infant through other modalities. We also suggest that bedsharing may minimize prone infant positioning, a known risk factor for SIDS. Am J Phys Anthropol 103:315–328, 1997. © 1997 Wiley-Liss, Inc.     

Nighttime Wakefulness Associated with Infant Rearing in Callithrix kuhlii

Parent-infant cosleeping occurs in human and nonhuman primates, yet studies on the impact of cosleeping on parental sleep patterns have been limited to human mothers. We examined the effects of cosleeping on the nighttime wakefulness of a biparental New World primate, Wied's black tufted-ear marmoset (Callithrix kuhlii). We compared the sleep patterns of marmoset parents caring for young infants to those without infants, using an 8 mm videocamera and timelapse VCR under infrared illumination. The presence of young infants significantly impacted the sleep of mothers but not fathers. In fact, mothers rearing young infants were awake >3 times as often as mothers without infants. We also examined the nighttime wakefulness of marmoset parents across the first 9 weeks of infant life (birth through weaning). Although callitrichid mothers tend to reduce their daytime investment in offspring very early in infant life by relinquishing the care of infants to fathers and alloparents, increased nighttime wakefulness was not limited to the early postpartum period for the mothers. Instead, mothers exhibited more nighttime wakefulness than fathers did across the first 9 weeks of infant life. Our results indicate that the presence of infants has a greater impact on the sleep patterns of Callithrix kuhlii mothers than fathers, suggesting that mothers are more involved in infant care than previously realized and that fathers are not nearly as involved in nighttime care as their behavior during the day would suggest.     

Evolved psychology in a novel environment

The human “environment of evolutionary adaptedness” can only be inferred indirectly. In contrast, the behavior of some nonhuman animals can be compared among “natural” and various altered environments. As an example, male immigration tactics in unprovisioned versus provisioned macaque (Macaca) populations are compared using Tooby and Cosmides’s (1992) framework for evolutionary functional analysis. In unprovisioned populations, social groups contain few males, and immigrant male takeovers of alpha rank occur frequently. In provisioned populations, groups contain many males, and males almost invariably enter social groups at very low rank and rise in rank only as more dominant males emigrate or die. Male conformity to the “seniority rule” is hypothesized to represent the behavioral output of an evolved decision-making algorithm (psychological mechanism) that takes into account (1) the net payoff of each rank in the dominance hierarchy and (2) the power of male group size as a predictor of the likelihood of successful immigrant takeover. Joseph H. Manson is Assistant Professor of Anthropology at the University of California, Los Angeles. His research interests are social relationships in nonhuman primates and humans, with particular emphases on mate choice, courtship tactics, intrasexual competition, and (currently) mother-infant relationships and infant handling. He has conducted fieldwork on rhesus macaques at Cayo Santiago and white-faced capuchins in Costa Rica.     

Where Will the Baby Sleep? Attitudes and Practices of New and Experienced Parents Regarding Cosleeping with Their Newborn Infants

An evolutionary perspective on human infant sleep physiology suggests that parent-infant cosleeping, practiced under safe conditions, might be beneficial to both mothers and infants. However, cosleeping is not part of mainstream parenting ideology in the United States or the United Kingdom, and little evidence is available to indicate whether, and under what circumstances, parents sleep with their newborn infants. We present data from an anthropological investigation into the practices and attitudes of new and experienced parents of newborn infants regarding parent-infant sleeping arrangements in a community in the northeast of England. Despite not having contemplated cosleeping prior to the birth, new parents in our sample found it to be a convenient nighttime caregiving strategy, and one which was practiced regularly. Infants slept with both their parents, some being habitual all-night cosleepers, but commonly beginning the night in a cnb and sleeping with their parents for several hours following the early morning feed, [infant sleep, newborn, cosleeping, new parents]     

Prenatal nicotine alters vigilance states and AchR gene expression in the neonatal rat: implications for SIDS

Maternal smoking is a major risk factor for sudden infant death syndrome (SIDS). The mechanisms by which cigarette smoke predisposes infants to SIDS are not known. We examined the effects of prenatal nicotine exposure on sleep/wake ontogenesis and central cholinergic receptor gene expression in the neonatal rat. Prenatal nicotine exposure transiently increased sleep continuity and accelerated sleep/wake ontogeny in the neonatal rat. Prenatal nicotine also upregulated nicotinic and muscarinic cholinergic receptor mRNAs in brain regions involved in regulating vigilance states. These findings suggest that the nicotine contained in cigarette smoke may predispose human infants to SIDS by interfering with the normal maturation of sleep and wake.     

Heart Rate Variability in Sleeping Preterm Neonates Exposed to Cool and Warm Thermal Conditions

Sudden infant death syndrome (SIDS) remains the main cause of postneonatal infant death. Thermal stress is a major risk factor and makes infants more vulnerable to SIDS. Although it has been suggested that thermal stress could lead to SIDS by disrupting autonomic functions, clinical and physiopathological data on this hypothesis are scarce. We evaluated the influence of ambient temperature on autonomic nervous activity during sleep in thirty-four preterm neonates (mean ± SD gestational age: 31.4±1.5 weeks, postmenstrual age: 36.2±0.9 weeks). Heart rate variability was assessed as a function of the sleep stage at three different ambient temperatures (thermoneutrality and warm and cool thermal conditions). An elevated ambient temperature was associated with a higher basal heart rate and lower short- and long-term variability in all sleep stages, together with higher sympathetic activity and lower parasympathetic activity. Our study results showed that modification of the ambient temperature led to significant changes in autonomic nervous system control in sleeping preterm neonates. The latter changes are very similar to those observed in infants at risk of SIDS. Our findings may provide greater insight into the thermally-induced disease mechanisms related to SIDS and may help improve prevention strategies.     

Generation of transgenic monkeys with human inherited genetic disease

Modeling human diseases using nonhuman primates including chimpanzee, rhesus, cynomolgus, marmoset and squirrel monkeys has been reported in the past decades. Due to the high similarity between nonhuman primates and humans, including genome constitution, cognitive behavioral functions, anatomical structure, metabolic, reproductive, and brain functions; nonhuman primates have played an important role in understanding physiological functions of the human body, clarifying the underlying mechanism of human diseases, and the development of novel treatments for human diseases. However, nonhuman primate research has been restricted to cognitive, behavioral, biochemical and pharmacological approaches of human diseases due to the limitation of gene transfer technology in nonhuman primates. The recent advancement in transgenic technology that has led to the generation of the first transgenic monkey in 2001 and a transgenic monkey model of Huntington’s disease (HD) in 2008 has changed that focus. The creation of transgenic HD monkeys that replicate key pathological features of human HD patients further suggests the crucial role of nonhuman primates in the future development of biomedicine. These successes have opened the door to genetic manipulation in nonhuman primates and a new era in modeling human inherited genetic disorders. We focused on the procedures in creating transgenic Huntington’s disease monkeys, but our work can be applied to transgenesis in other nonhuman primate species.     

Birth intervention and non-maternal infant-handling during parturition in a nonhuman primate

Direct intervention in infant delivery by non-parturient individuals is a rare phenomenon in nonhuman primates. In contrast, birth assistance by other individuals, or the practice of midwifery, is universal among human societies and generally believed to be a behavior unique to our species. It has been proposed that the enlarged head of the human fetus and the relatively narrow birth canal constrained by bipedalism has made human parturition more difficult than in nonhuman primates, and these anatomic challenges have led to the rotation of the fetus in the birth canal and an occiput anterior (i.e., backward-facing) orientation of emergence. These characteristics have hindered the mother’s ability to self-assist the delivery of the infant, therefore necessitating assistance by other individuals or midwives for successful birth. Here we report the first high-definition video recordings of birth intervention behavior in a wild nonhuman primate, the white-headed langur (Trachypithecus leucocephalus). We observed that while a primiparous female gave birth to an infant in an occiput posterior (i.e., forward-facing) orientation, a multiparous female intervened in the delivery by manually pulling the infant out of the birth canal and cared for it in the following hours. Our finding shows extensive social interactions throughout parturition, and presents an unequivocal case of non-maternal intervention with infant birth in a nonhuman primate.     

The protective effect of breast feeding in relation to sudden infant death syndrome (SIDS): II. The effect of human milk and infant formula preparations on binding of Clostridium perfringens to epithelial cells

Breast feeding is known to protect an infant against gastrointestinal pathogens and epidemiological studies indicate that compared to breast fed infants, formula fed infants are at a greater risk of dying from sudden infant death syndrome (SIDS). Many SIDS infants have symptoms of gastrointestinal infections prior to death and one gastrointestinal pathogen associated with SIDS is Clostridium perfringens. Studies have found that a significantly higher number of formula fed SIDS infants have C perfringens and its enterotoxin in their faeces compared to breast fed infants. The aim of the study was to compare the effects of human milk and infant formula on binding of C perfringens to epithelial cells. Two protocols were used to assess the effect of human milk and infant formula to inhibit binding of C perfringens to epithelial cells. Binding was assessed by flow cytometry. For the in vivo protocol which more closely represents interactions on the mucosal surface, breast milk enhanced bacterial binding but infant formula caused inhibition of binding; however for the in vitro method, both human milk and infant formula resulted in consistent enhancement of binding. Flow cytometry studies indicated that enhancement of binding was due to the formation of bacterial aggregates. Lewis(a) and Lewis(b) antigens, found in both breast milk and infant formula, inhibited C. perfringens binding in a dose dependent manner. The Lewis(a) and Lewis(b) antigens in human milk and infant formula can inhibit C. perfringens binding to epithelial cells. While infant formula reduced binding of C. perfringens to epithelial cells in the experiments carried out with the in vivo protocol, the protective effects of breast feeding in relation to colonisation with C. perfringens are more likely to be due to formation of bacterial aggregates. These findings have implications for improving infant formula preparations.     

Parent-infant bed-sharing behavior

An evolutionarily informed perspective on parent-infant sleep contact challenges recommendations regarding appropriate parent-infant sleep practices based on large epidemiological studies. In this study regularly bed-sharing parents and infants participated in an in-home video study of bed-sharing behavior. Ten formula-feeding and ten breast-feeding families were filmed for 3 nights (adjustment, dyadic, and triadic nights) for 8 hours per night. For breast-fed infants, mother-infant orientation, sleep position, frequency of feeding, arousal, and synchronous arousal were all consistent with previous sleep-lab studies of mother-infant bed-sharing behavior, but significant differences were found between formula and breast-fed infants. While breast-feeding mothers shared a bed with their infants in a characteristic manner that provided several safety benefits, formula-feeding mothers shared a bed in a more variable manner with consequences for infant safety. Paternal bed-sharing behavior introduced further variability. Epidemiological case-control studies examining bed-sharing risks and benefits do not normally control for behavioral variables that an evolutionary viewpoint would deem crucial. This study demonstrates how parental behavior affects the bed-sharing experience and indicates that cases and controls in epidemiological studies should be matched for behavioral, as well as sociodemographic, variables.     

Change in immunisation schedule and sudden infant death syndrome in Hungary

Infant mortality in Hungary was higher than in other European countries; however, the reported incidence of sudden infant death syndrome (SIDS) has been lower than those for Western Europe and the United States. Childhood immunisation has been reported to be a protective factor for SIDS. In Britain, the change to an earlier immunisation schedule for diphtheria, pertussis, and tetanus appeared to be associated with a shift in the age distribution of SIDS. In 1999, immunisation for Haemophilus influenzae type b (Hib) was introduced for Hungarian infants at the age of 2 months. Data for total infant mortality and SIDS in Hungary were analysed between 1990 and 2002. Infection was the major cause of death among Hungarian infants followed by SIDS. Following introduction of Hib immunisation, there was a decrease in deaths due to meningitis from an average of 3.5% of all infant deaths between 1990 and 1998 to an average of 1% of all infant deaths between 1999 and 2002 (p=0.00). There was also a significant decrease in the proportion of SIDS in the age range > or =2 months from 48% in the earlier period to 39% after introduction of the vaccine (p=0.03). The decrease in SIDS might be due in part to decrease in unrecognised Hib infections or to induction of antibodies by the tetanus toxoid to which the Hib polysaccharide is conjugated that are cross reactive with bacterial toxins implicated in SIDS.     

An Exploratory Study of Human–Dog Co-sleeping Using Actigraphy: Do Dogs Disrupt Their Owner’s Sleep?

ABSTRACT

This exploratory study aimed to contribute to the limited research on human–animal co-sleeping by investigating the extent to which human sleep is disturbed by co-sleeping with a dog. Five female Australian dog owners and their dogs were fitted with activity monitors for seven nights. Raw activity of the dog and human for each sleep episode were matched and then compared using a time series correlation. Dog movement was a significant leading indicator of human movement, with dog activity positively indicating human activity up to 2.5 minutes in advance. Dogs were active for about 20% of the night, with humans 4.3 times more likely to be awake during dog activity than during dog inactivity (10.55%/2.45%). Co-sleeping appears to cause sleep disturbances (both arousals and wake ups), which is reinforced by poor scores on validated sleep measures. There also appears to be disparity between these objective measures and subjective evaluations of sleep quality and number of disturbances. At least in the small sample considered in the present study, co-sleeping with a dog appears to result in measurable, but relatively mild, reductions in overall sleep quality. This detrimental impact must be weighed against the benefits of co-sleeping.     

Clostridium perfringens type A cytotoxic-enterotoxin(s) as triggers for death in the sudden infant death syndrome: Development of a toxico-infection hypothesis

In our studies with the pathogenic bacteriumClostridium perfringens type A and its cytotoxic-enterotoxins (CTEs), we have obtained results that imply an involvement of this organism in the sudden infant death syndrome (SIDS). In fecal samples obtained from SIDS infants (n=164) and non-SIDS infants (n=57),C. perfringens type A was present in high numbers in >80% of SIDS and <2% of control non-SIDS cases respectively. Fecal samples from SIDS infants analyzed by ELISA forC. perfringens type A CTEs showed a very strong positive correlation with the presence of the organism. Histopathological examination of ileal tissue from SIDS infants showed remarkable similarity to tissue from animal models affected byC. perfringens type A CTEs, where the patterns of damage were positively correlated with the age of the animal. We propose that systemic distribution of the CTEs acts parasympathomimetically to trigger a biochemical cascade that alters cardiorespiratory control. Death may subsequently ensue in an immunologically vulnerable infant.Florida Agricultural Experiment Station Journal Series No. R-02419.     

Interactions between parents and infants,and the development of independence in the common marmoset (Callithrix jacchus)

Detailed observations were made of the parent-infant interactions of five adult pairs and 31 infant common marmosets (Callithrix jachus), housed in captive family groups. Records of parental measures were taken up to 4 months old and comparisons made between infants in similar social situations. These comparisons investigate sex differences, birth-order variations, those between singleton and twin infants, parental variation and the proportion of time that older siblings carry infants. Correlations between the measures reveal that both parents are responsible for promoting and regulating increasing infant independence. In the discussion, comparisons are made with other parent-infant studies and problems of the adaptiveness of the Callitrichid social system considered.     

The meaning of character combination for the separation of EEG-data

Summary Standard EEG risk evaluation works on scoring systems that use different types of questionnaires. Here, an alternative for SIDS (Sudden Infant Death Syndrome) risk detection is presented that is based exclusively on EEG data which possibly could substitute the procedure of questioning the parents and allow a direct qualification of the physiological disposition of the individual neonate: Using EEG-characters an approved SIDS-case could be discriminated as well against the group of “healthy” infants as against the “high-risk-group”. The results of this study may confirm the evidence that the EEG analysis can be a promising approach to predict an increased SIDS risk.