Appropriate thermal protection of the newborn prevents hypothermia and its associated burden of morbidity and mortality. Yet, current global birth practices tend to not adequately address this challenge. Here, we discuss the pathophysiology of hypothermia in the newborn, its prevention and therapeutic options with particular attention to resource-limited environments. Newborns are equipped with sophisticated mechanisms of body temperature regulation. Neonatal thermoregulation is a critical function for newborn survival, regulated in the hypothalamus and mediated by endocrine pathways. Hypothermia activates cellular metabolism through shivering and non-shivering thermogenesis. In newborns, optimal temperature ranges are narrow and thermoregulatory mechanisms easily overwhelmed, particularly in premature and low-birth weight infants. Hyperthermia most commonly is associated with dehydration and potentially sepsis. The lack of thermal protection promptly leads to hypothermia, which is associated with detrimental metabolic and other pathophysiological processes. Simple thermal protection strategies are feasible at community and institutional levels in resource-limited environments. Appropriate interventions include skin-to-skin care, breastfeeding and protective clothing or devices. Due to poor provider training and limited awareness of the problem, appropriate thermal care of the newborn is often neglected in many settings. Education and appropriate devices might foster improved hypothermia management through mothers, birth attendants and health care workers. Integration of relatively simple thermal protection interventions into existing mother and child health programs can effectively prevent newborn hypothermia even in resource-limited environments.
The need for thermal newborn protection has long been known, as alluded to by Soranus of Ephesus (98 to 138 AD) in his four-volume treatise ‘On Diseases on Women’, which demonstrates the importance of keeping newborns warm.1 The Bible provides probably the most well-known example of thermal protection of the newborn in Luke 2: 7, ‘And she brought forth her firstborn son, and wrapped him in swaddling clothes, and laid him in a manger.’
Yet, in current times, the majority of the almost 4 million newborns globally who do not survive their first month of life2 die of complications associated with hypothermia, such as prematurity and severe infections (mostly sepsis and pneumonia).3 As two recent reviews have acknowledged, neonatal deaths related to hypothermia are relatively neglected, but considered easily preventable with attention to warmth, feeding and infection management.4, 5 This article focuses on the diagnosis of hypothermia and management of thermal protection of newborns in low-resource environments. We review mechanisms of neonatal thermoregulation, discuss the pathophysiology of newborn hypothermia and present simple strategies of thermal protection for the newborn.
The normal body temperature of a newborn infant is usually defined as ranging between 36.5 and 37.5 °C (97.7 to 99.5 °F).6 A series of observational randomized trials starting in the late fifties7, 8 showed that keeping babies warm reduces mortality and morbidity, and spurred further research on the pathophysiology of thermoregulation in newborns. Thermoregulation is a biological priority for all homeothermic species.9 Newborns, particularly preterm and low-birth weight (LBW) infants, have limited capacity for thermoregulation during the first weeks of life. The optimal environmental temperature is termed thermal neutral temperature, at which metabolic requirements of the organism are minimal.10 Both a decreased and an increased core temperature increase the metabolic rate of newborns,11 who have only very limited ability to maintain a normal temperature and easily become hypothermic or hyperthermic. Although hyperthermia also increases energy needs, hypothermia seems to carry a higher risk of complications.12
When the infant's body temperature decreases in response to sudden exposure to cold extrauterine environments, signals from peripheral and central thermoreceptors reach the hypothalamus through afferent pathways.13 The resulting norepinephrine release then triggers nonshivering thermogenesis, or lipolysis of brown adipose tissue, which is the main homeothermic heat production mechanism in newborns. Heat production occurs through uncoupling ATP synthesis via the oxidation of fatty acids in the mitochondria, utilizing uncoupled protein.14
Afferent temperature information is processed in the hypothalamus. Thermoregulation requires an intact central nervous system,15 and impaired thermoregulation, either hypo- or hyperthermia, can be indicators of central nervous system damage. The hypothalamus has a central role in regulating the autonomic, somatic and endocrine systems to maintain a normal body temperature. Decreasing body temperatures trigger a release of thyroid-stimulating hormone, which leads to an increase in thyroxine and consequently triiodothyronine. The resulting norepinephrine release causes vasoconstriction, glycolysis and uncoupling of mitochondrial oxidation in the brown adipose tissue, further generating heat production.14 The latter process is ineffective in preterm infants, because it depends on the amount of brown fat as well as levels of the enzymes 5′/3′-monodeiodinase and thermogenin, which build up only later in fetal development.13
Shivering is not regularly involved in a newborn's reaction to cold stress.16 Another mechanism of heat production is infant behavior:10 the irritable baby prompts the mother to hold the baby, drying, cuddling and swaddling him or her, thus preventing heat loss.
Newborns are unable to maintain their body temperature on their own without thermal protection. Although a newborn's thermoregulation is as complex as in adults if not more sophisticated, as discussed above, their range of optimal or even tolerable body temperature is narrower. A newborn placed naked in an environment of 23 °C at birth suffers the same cold as does a naked adult at 0 °C.17 Without thermal protection, human neonates are functionally poikilothermic, that is, they change their body temperature according to environmental temperatures. In newborns placed in a colder environment, core temperature decreases at a rate 0.2 to 1.0 °C per minute and finally may lead to death from cessation of metabolic activities.10
Pathophysiology of newborn hypothermia
The World Health Organization (WHO) defines neonatal hypothermia as a temperature below 36.5 °C (97.7 °F) and proposes the following classification:17 Mild hypothermia, caused by cold stress, is classified as a body temperature range from 36 to 36.5 °C (96.8 to 97.7 °F) and is considered a cause for concern,17 because the exposed infant begins to lose more heat than he or she can produce.13 Moderate hypothermia is a body temperature from 32 to 36 °C (89.6 to 96.8 °F), indicating danger and requiring warming of the baby. According to the WHO classification, a body temperature of <32 °C (89.6 °F) is considered severe hypothermia, or cold injury, with a potentially grave outcome, and needs immediate skilled attention.
Heat loss occurs in several ways. The most common scenario is that of a wet baby who is not dried, and in whom evaporation of fluid from the skin leads to heat loss. Evaporation often occurs with amniotic fluids during the first minutes of life or with water after a baby is bathed. The energy loss is substantial: immediately at delivery, when the environmental temperature surrounding the baby drops from 37 °C in the maternal womb to the usually less warm air temperature, evaporative heat loss begins at a rate of 0.58 kcal ml−1 fluid evaporated.10
A baby placed naked on a cold surface loses heat through conduction. A newborn exposed to cool surrounding air or draughts will lose heat through convection. Radiation from cool objects next to the baby (for example, a cold wall) can also lower its body temperature. Unlike in adults, sweat secretion has little or no role in the thermoregulation of a newborn or preterm baby.18
As all data on hypothermia are from observational studies and prospective randomized trials without treating hypothermia are not permissive, the direction of causality for factors associated with hypothermia is not entirely clear.
Some argue that lowering body temperatures might increase metabolic processes to generate heat, which could lead to hypoglycemia and hypoxia in response to increasing energy demands.13 As hypothermia and hypoglycemia both exacerbate hypoxia, this would reinforce a vicious circle19 and could on one hand explain the mortality associated with hypothermia. However, studies have shown that hypothermia is not a risk factor for neonatal hypoglycemia in analyses adjusted for confounders such as LBW or anemia.20 On the other hand, hypoglycemia is common among newborns in resource-limited settings20 and, instead of being a consequence, could rather be a cause of hypothermia.
Similarly, with regard to the reported associations of hypothermia with infections and organ failure,21, 22 hypothermia might be either a consequence or a cause of severe infections. Clinically, hypothermia is an indicator for severe infections analogous to hyperthermia, or fever. In fact, neonatal hypothermia is associated in an unclear direction of causality with various pathologies such as surfactant inactivation, increased morbidity from infection, abnormal coagulation, delayed readjustment from the fetal to newborn circulation, hyaline membrane disease and intraventricular hemorrhage in LBW infants.23
In contrast, mild therapeutic hypothermia has emerged as a neuroprotective strategy in the treatment of hypoxic ischemic encephalopathy. Recent randomized controlled trials have shown that therapeutic hypothermia initiated within 6 h of birth reduces death and disability in these infants.24 Induced under controlled clinical conditions, therapeutic hypothermia has been discussed as being beneficial and outweighing the adverse effects in term newborns with hypoxic ischemic encephalopathy25 and during or after cardiac surgery.26
Heat is transferred in utero via the placenta through umbilical arterial blood flow and via the uterus through amniotic fluid to the fetus.14 At birth, fetal temperature is usually 0.5 to 1.0 °C higher than the mother's27 and increases not only with elevated maternal temperatures due to prolonged labor, prolonged rupture of the membranes or other infectious etiologies (chorioamnionitis, urinary tract infection, and so on), but also with nulliparity and epidural analgesia.28
The most common cause of elevation of body temperature in the newborn is dehydration.29 Rehydration is both therapeutic and diagnostic if the newborn improves. Elevated temperatures in the neonate rarely reflect intrauterine or perinatal infections. Among the 1 to 2.5% of newborns presenting with hyperthermia, <10% have culture-proven sepsis.10 In septic newborns, temperature instability more frequently presents as hypothermia. The exact mechanisms that lead to fever in some septic neonates and normal body temperatures in others are ill understood. Infection is thought to produce fever mediated through cytokines such as interleukin1. Antipyretics are effective in reducing the temperature by modifying the central set-point of the hypothalamus. In hyperthermia due to environmental overheating, antipyretics are ineffective, and newborns are appropriately managed by reducing the environmental heat exposure.
Central malformations and intracranial hemorrhages, or congenital pathologies such as the Crisponi syndrome,30 are rare causes of newborn hyperthermia.
Where thermoprotective devices are used, inappropriate incubation and exposure to radiant warmers are common causes of neonatal hyperthermia,10 especially when makeshift apparatuses such as light bulbs, hot stones, and so on, are used. These are usually not designed and tested for safety and efficiency, and we discourage their use in favor of skin-to-skin care (SSC).
Management of newborn hypothermia
Qualitative inquiries into current thermal practices
Although lack of equipment is a problem for high-risk neonates in resource-poor settings, knowledge of hypothermia diagnosis and management is another concern. For example, only about half of 160 surveyed health care professionals in India could define neonatal hypothermia correctly or considered it a significant problem, and <20% knew how to correctly record a newborn's temperature.31 A multinational study showed that knowledge on thermal control, especially concerning the physiology of thermoregulation and criteria for defining hypothermia, was insufficient and thermal control practices were frequently inadequate.23
Qualitative research on newborn care can help shed light on the beliefs and attitudes underlying potentially detrimental or harmful practices. Most published studies indicate that high-risk home delivery and newborn care practices that lead to heat loss, such as insufficient heating of the birthplace, placing of the uncovered newborn on the ground or other cold surfaces, delayed wrapping—partly with unclean clothes—and early bathing, remain common in resource-limited settings both in rural and urban areas, in facilities and during home births.5, 32, 33
Heating the birthplace is a critical issue for home births. Studies from Nepal reported that the birthplace was heated in only slightly over half of the settings,34 often only after birth.35 Wrapping the child prevents heat loss from evaporation, whereas bathing promotes heat loss. Less than half (46%) of the babies were wrapped within the first 10 min after birth, and almost all of them were bathed within 10 min (89%) or half an hour (96%) after birth.34 In another study, only 64% of the babies were observed to be wrapped within half an hour after birth, and almost all were bathed within 6 h after birth.35
In a study from Tanzania, the practice of bathing newborns immediately after delivery was shown to be motivated by concerns about ‘ritual pollution’.36 In Ghana, early bathing was linked to reducing body odor in later life, shaping the baby's head, and helping the baby sleep and feel clean, and informants felt that changing bathing behaviors would be difficult, especially as babies are bathed early in facilities.37 A study from Dhaka, Bangladesh, explained that babies are typically bathed soon after birth to purify them from the birth process.38 Several studies, from Uganda,39 Ghana37 and India40 suggested that in the absence of health facilities prepared to deliver essential newborn care, community members would accept thermoprotective practices such as SSC.
It has been estimated that prompt recognition of hypothermia and re-warming of hypothermic infants will avert up to 40% of neonatal deaths.41 Newborn hypothermia presents with a combination of low core temperature and cold skin, pallor (acrocyanosis), tachypnea (respiratory distress), hypotonia, lethargy or irritability, poor feeding or vomiting. The non-specific clinical presentation and the complex process of thermoregulation discussed above imply a number of differential diagnoses such as infectious etiologies, respiratory distress syndrome, intraventricular hemorrhage or other central nervous causes, hypoglycemia, endocrine causes, or (maternal) drug side effects. Other factors potentially underlying hypothermia include prematurity, cardiovascular diseases and other congenital anomalies.
Initial assessment should include a history of the baby's exposure to cold and whether the baby has been appropriately clothed and protected.18 Although a rectal digital thermometer is used in many studies as standard method to measure a newborn's core temperature, this measurement site is associated not only with discomfort and disturbance to the newborn, but also with risks such as rectal perforation and vagal stimulation with resulting arrhythmias, bradycardia and apnea.42
The axilla is a less invasive, alternative site that provides reasonably accurate measurements. Mercury-in-glass, gallium-in-glass, digital thermometer, analogous electric thermometer, chemical thermometer and infrared thermometer are all accurate instrument options, with the latter being less hazardous and quicker than the former.43 Most developed institutions use tympanic thermometers, which have recently shown to be a quick and accurate method to measure a newborn's body temperature,44 whereas simple rectal thermometers are used in most resource-limited settings. WHO recommends frequent measurements, from every hour in a seriously ill baby, two to four times per day in a small or very small baby, to once daily in an infant progressing well.18 However, due to their cost, thermometers are often not available in low-resource environments. Moreover, illiteracy and inability to read Arabic numbers have been a challenge to thermometer use.
In the absence of a measurement device, human touch of feet and abdomen has been used as a proxy for body temperature. Studies in India and Nepal have shown human touch to be reasonably reliable for the detection of hypothermia when health workers were trained for these investigations.45, 46, 47, 48, 49 Mothers, however, seem to have a far lower sensitivity than health workers. Only 24% of mothers in India were able to correctly identify hypothermia.50
A device based on color indicators developed to detect hypothermia without the use of thermometers was previously found to accurately indicate hypothermia when used by health workers or mothers.51, 52 Its usefulness for some parts of the developing world and the feasibility for illiterate health workers to read the device have been debated.53, 54
Therapeutic goals of thermal care
The therapeutic goal of thermal care is to keep the newborn in the thermoneutral zone, or thermal neutrality, the environmental temperature range in which the organism has least oxygen consumption.9 No single environmental temperature is optimal for all babies. In general, the smaller and more premature a newborn is, the less its ability to regulate cold and heat. The optimal environmental temperature thus depends on the maturity (usually estimated by the gestational age) and age of the newborn. Weight, body temperature and skin perfusion as well as clothing of the infant and air humidity also factor in, so that the optimal environmental temperature can be hard to determine. It is narrow, especially in LBW or sick babies, and generally ranges from 32 to 36 °C.55 It follows that a temperature appropriate for a healthy term baby can be too cold for a preterm infant (and, conversely, what is appropriate for the preterm infant can be too warm for the term baby). In general, most newborns at birth, if left wet and naked, cannot tolerate an environmental temperature of <32 °C. However, if the baby is immediately dried, put skin-to-skin with the mother and covered, the delivery room temperature can be as low as 25 to 28 °C.17
Prevention of newborn hypothermia
WHO recognizes maintaining a normal body temperature as a primary principle of newborn care and recommends thermal protection for all infants, with special attention for sick, premature, or small for gestational age infants, for example, <2.5 kg at birth or born before 37 weeks gestation.18 Several methods can be used for warming the baby and maintaining the baby's body temperature (Table 1). The WHO proposes a ‘warm chain’, a set of 10 interlinked procedures carried out at birth and during the following hours and days. To be implemented in institutions and (in an abridged form) at home, the warm chain aims to minimize the risk of hypothermia in newborns, and includes warming the delivery room, immediate drying, SSC, early and exclusive breast-feeding, postponing bathing, appropriate clothing and bedding, placing mother and baby together, and in institutions warm transportation, warm resuscitation, and training and awareness raising.17
WHO recommends warming the delivery place in preparation for a birth (to at least 25 °C) and to keep the birthplace free from draughts. After delivery, it is crucial to devote some attention to the baby. The first and most substantial heat loss occurs through evaporation of amniotic fluid. Therefore, at birth, recommended first steps to prevent hypothermia are to immediately dry and cover the newborn, even before the cord is cut. While being dried, the baby should be on a warm surface, preferably the mother's chest or abdomen in skin-to-skin contact. The infant should then be clothed or covered, especially the head,56 and kept in a warm environment, again usually best with the mother. Bathing should be delayed. Draughts, cold surfaces or nearby cold sources such as windows or walls should be avoided as they contribute to heat loss via convection and radiation.
Early breastfeeding, ideally within an hour after delivery, should be encouraged if possible and if not contraindicated. SSC with the mother, for LBW infants also known as kangaroo mother care, most of the time is appropriate to ensure thermal protection of the baby.57 It requires minimal instructions and, when culturally accepted, can relatively easily be applied even in a community or home setting.58
Treatment of newborn hypothermia
According to current WHO guidelines for the treatment of cold babies, moderate hypothermia should be treated by SSC.18 In severe hypothermia, rewarming the baby with an appropriate and available method in a health care facility setting is warranted, as close monitoring of vital signs including temperature and respiratory rate are essential parts of the management. Blood glucose should be controlled and hypoglycemia under 45 mg dl−1 (2.6 mmol l−1) should be treated accordingly. When treating for sepsis, all IV fluids should be given warm. The infant can be discharged once a stable normal temperature is sustained and there are no other issues. Upon discharge, the mother should be counseled to prevent hypothermia at home as discussed above.
There is a relative scarcity of data documenting the effects of recommended thermal newborn care. A recent meta-analysis showed that SSC in conjunction with breastfeeding and recognition of danger signs substantially reduced neonatal mortality in hospital-born preterm babies (birth weight <2000 g) in hospital, and was highly effective in reducing severe morbidity, particularly from infection.59 A study from Western India, in which 36.9% of hospitalized newborns were hypothermic, reported a decrease in this rate to 3.9% with kangaroo mother care.60 However, in many countries there is resistance from health professionals, mothers and families related to local cultural practices.61 Although evidence on the effectiveness of SSC in community-based settings is scarce,40, 62 it is estimated that SSC can avert up to 20% of newborn deaths.63
In the large Gadchiroli trial in India on home-based neonatal care assessing the outcome of sepsis management, case management included thermal protection of the newborn, and health care workers were given a thermometer, baby clothes and head cover, a blanket and a sleeping bag. Although the study included other interventions and was not specifically designed to prove a particular effect for hypothermia management, it showed a reduction in neonatal and infant mortality by nearly 50% among a malnourished, illiterate and rural study population.64 A study from Nepal that found a high incidence of hypothermia suggests that simple interventions including immediate drying and another treatment (breast contact, radiant heater and mustard oil massage, or swaddling with an inner layer of plastic wrap) could lower the incidence of hypothermia 2 h after birth from 78 to 23% and 24 h after birth from 49 to 18%.65 In Zambia, we recently showed that training traditional birth attendants in newborn care with special emphasis on resuscitation and simple thermal protection (wiping the newborn dry and wrapping the dried infant in a separate piece of cloth) along with an intervention to provide early treatment of possible sepsis reduced mortality rates at day 28 after birth by 45%.66
Low-cost, low-tech treatment of newborn hypothermia
The use of incubators for thermal protection of newborns has been reported for more than 150 years, since the Parisian obstetrician Jean Louis Paul Denucé in 1857 engineered his couveuse, a device for the care of a premature infant. In 1878, his local colleague Stéphane Tarnier, using a modified warming chamber for the rearing of poultry, found a decrease in neonatal death rate from 66 to 38% among infants with birth weights <2000 g.67
Today, postnatal care devices (isolettes or infant warmers) combine the features of incubators and radiant warmer beds and have evolved with many features, including automated temperature and humidity regulations,68 oxygen supplementation and light therapy.11, 69 Although beneficial in resource-replete settings,70 utilization of their complex features requires electricity, concentrated oxygen supply, centralized suction and ongoing skilled maintenance. Priced at about US$15 000 to $36 000,71 these devices are not affordable for most of the developing world. Simplified versions, such as water-filled mattresses or Indian made, low-cost radiant warmers are power-dependent and not appropriate for resource-limited settings. Polyethylene occlusive skin wrapping is a useful and effective method for delivery room management,72 but mostly limited to immediate post-delivery care and protection during transport.
A number of postnatal care devices for resource-limited settings are currently in development, some including more sophisticated temperature and humidity regulations. Examples are the ‘mkat,’ ‘Life Raft Incubator,’ and ‘Neo.nurture’, projected to be priced between US $200 and US $625 per unit.73 The ‘Embrace Global’, projected to be priced at a US $25 price, is a life vest style incubator in a ‘sleeping bag’ design.74 The heat source is a pouch-containing phase change material, which keeps its temperature relatively constant over an extended period of time. The pouch is warmed electrically or by the user simply pouring hot water into a compartment, upon indication by a thermal strip. It can fully open to double as a heat mattress. With some models electricity independent, it can be used both at the institutional and community levels, and serve as visual reminders to mothers and other caretakers, birth attendants and health care workers. Devices such as these, although more costly than education alone, might thus foster improved hypothermia management by transporting a behavioral message to the end user, for example, promoting SSC. Distributed commercially or donated, they could help to raise awareness and enhance perception of the burden of newborn hypothermia.
Thermal protection of the newborn can relatively easily be achieved by warming of the delivery room, immediate drying, wrapping the infant after birth and keeping him or her in close contact with the mother, that is, kangaroo mother care or SSC, immediate and frequent exclusive breastfeeding, delaying of bathing until the infant is physiologically stable, and appropriate warm clothing. These behavior steps represent simple, low-cost measures, which should be integrated into holistic mother and child health packages.
Birth practices even in high-risk environments remain poor, so that interventions must primarily focus on participatory education about hygiene, infection prevention and management, as well as practices to avoid hypothermia. Low-cost, low-technology devices might be helpful in supporting and implementing these practices. Clinical effectiveness and implementation trials will have to investigate which intervention packages and messages for the thermal protection for newborns work best in a given environment, and how to optimally integrate them into existing maternal and newborn health programs.
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The authors declare no conflict of interest.
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Lunze, K., Hamer, D. Thermal protection of the newborn in resource-limited environments. J Perinatol 32, 317–324 (2012). https://doi.org/10.1038/jp.2012.11
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