More than 50 years after Silverman showed the association between temperature control and mortality, recent data again stress the importance of the thermal environment of the preterm infant. The goals of care are straightforward: maintain a normal body temperature, ensure a stable thermal environment and avoid cold stress; but the options to achieve them are many and less certain. There is a problem in defining a ‘normal’ temperature. A single measurement will tell nothing about whether the baby is using energy for thermal balance. The preterm baby should be monitored with the continuous recording and display of a central and peripheral temperature. This will give an early indication of cold stress before any change is seen in the central temperature. Reducing evaporative heat losses at birth has improved temperatures on admission, although no studies have shown any effect on outcome. No data have shown that the use of incubators is any better than radiant heaters.
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The importance of keeping newborn babies warm has been known for centuries but it was not until the 1950s that Silverman and colleagues1 2 showed, in a series of randomised controlled trials, the clear link between incubator humidification, temperature control and neonatal mortality across all birth weight groups.
Recommendations for environmental temperature settings were developed using the concept of the neutral thermal environment,5 and these were further developed through the 1980s.6 By the 1990s there was literature comparing babies nursed in incubators and under radiant heaters7 and reviews of the use of semipermeable membranes8 and emollients9 to prevent TEWL. The impression at that time was that thermoregulation of the newborn was thought to be understood and being managed well.
In the early 2000s studies revealed poor temperature management of the immature baby during vulnerable times,10 and for the very immature baby the admission temperature was shown to be inversely related to mortality (28% increase per 1°C)11 12 and late onset sepsis.12 It is clear, more than 50 years after the work of Silverman and colleagues,1 2 that thermal control, particularly of the immature infant, is still an important issue in need of further thought and study.
Vulnerability of the preterm baby
The temperature of the fetus is between 0.5°C and 1°C higher than that of the mother.13
Although some heat loss after delivery may be important in stimulating metabolic adaptation it is important to avoid a continuing drop in body temperature.14 This can be achieved in the healthy term baby by drying and wrapping, applying a hat, or using skin-to-skin care. The preterm baby though often needs a period of stabilisation and has traditionally been placed naked on a resuscitaire.
The baby exchanges heat with its environment through radiation, convection, conduction and evaporation. The immature baby is at high risk of net heat loss because of a high surface area to volume ratio and increased evaporation of fluid from the skin. Mechanisms of heat production are limited as is the ability to reduce heat loss by peripheral vasoconstriction.15 Given these physiological limitations, the goal of care of the preterm baby is to maintain a normal body temperature and minimise thermal stress, particularly cold stress.
A number of strategies are used to try and achieve a thermoneutral state for the baby. However, in order to evaluate their effectiveness it is important to understand temperature measurement techniques.
There are two problems with temperature measurement. First is a problem in trying to define a ‘normal’ temperature as this will depend very much on where, and possibly how, it is being measured. There is no such thing as a single central temperature, with tissues varying depending on their metabolic rate.16 Second, a normal central temperature does not mean the baby is in a thermoneutral state. A baby may be expending a vast amount of energy to maintain a normal temperature and yet be stressed thermally.17 In addition, the very low birth weight baby may demonstrate characteristics of a poikilotherm and show a temperature that drifts up and down, matching changes in the ambient temperature.15
Normal temperature ranges for newborns have not been clearly established. A published range for rectal and axillary temperatures is 36.5–37.5°C and 35.6–37.3°C, respectively, for both term and preterm infants; the skin temperature is 35.5–36.5°C in term babies and 36.2–37.2°C in preterm babies.18 Sauer et al6 suggest that conditions for thermoneutrality are met in very low birth weight infants when at rest their core temperature is between 36.7°C and 37.3°C and the core and mean skin temperatures are changing less than 0.2–0.3°C/h, respectively.
Modes of measurement
Various techniques and body sites have been used to provide an estimate of body core temperature.
Electronic thermometers may be used in manual and predictive mode. In predictive mode they give a rapid reading but the neonatal algorithms used have never been validated in the preterm population in large pragmatic trials.
Infrared technology is being used in the development of ear and skin thermometers. Tympanic temperature measurement has gained popularity in children, but in the newborn it reflects central temperature poorly due to technical difficulties related to the size of the ear canal.19 The literature on forehead and temporal artery thermometry in the newborn is limited.20 21
The usual sites used to the determine temperature of the newborn are the axilla, rectum and skin. Axillary temperature is usually measured intermittently and has little associated risk. Error in measurement is observed depending on the placement of the probe, adequate closure of the axillary pit, blood flow to the axillary region and possibly activation of non-shivering thermogenesis.22,–,24
Rectal temperature provides an approximation of core temperature but this mode has a risk of trauma. Reproducibility is uncertain; possible causes of inaccurate rectal readings include the value depending on the depth of insertion, dwell time, whether the baby has just passed stool and on the flow and temperature of the blood returning from the lower limbs.25 26
Probes attached to the skin are used for continuous temperature monitoring. A close approximation to deep body temperature can be achieved using the ‘zero heat flux’ technique.27 If a probe is placed over an area of skin from which no heat can be lost then, with heat flow down a temperature gradient from the centre of the body to the periphery, this area of skin will equilibrate with the deep body temperature. This can be achieved with a probe placed between the scapulae and a non-conducting mattress.
The intermittent measurement of a single temperature tells how well the baby is maintaining that temperature, but nothing about the energy being used to achieve thermal balance. Just because the measured temperature is acceptable does not mean that the environment is adequate, with the baby using energy to overcome the effects of thermal stress. The continuous measurement, and display, of central (abdominal, axilla or zero heat flux) and peripheral (sole of the foot) temperatures detects thermal stress by showing a change in the central–peripheral difference that occurs before any alteration in central temperature. The preterm baby who appears to be comfortable in its environment has a central temperature in the normal range for whichever site is being used and a central–peripheral temperature difference of 0.5–1°C. An increasing central–peripheral temperature difference, particularly above 2°C, is usually caused by cold stress and occurs before any fall in central temperature.28 A high central temperature, particularly if unstable, along with a wide central–peripheral gap is seen in septic babies.29
The sick immature baby should have continuous dual temperature monitoring. In the stable, growing preterm infant it is traditional to measure temperature, often axillary, at regular intervals. This will give limited information about the thermal state but may be important when there are concerns about poor growth or other signs of illness.
Options for achieving these goals
Delivery, stabilisation and transport
In the delivery room the baby is at risk of heat loss from conduction, convection, radiation and, of particular importance in the preterm, evaporation. To limit these losses the baby is usually dried and managed in a warm room with an ambient temperature of approximately 25°C, the mattress on which baby is placed is non-conducting and there is an additional heat source by way of a radiant heater. A hat is applied to the baby. However, studies have shown that despite these measures many preterm babies are cold on arrival in the neonatal unit.11 12 The use in recent years of polyethylene occlusive skin wraps or plastic bags is effective in reducing TEWL30 and, in babies under 28 weeks' gestation, results in higher temperatures on admission.31 32
Although the lowest acceptable admission temperature is not known, it is suggested that temperatures should be above 36°C in babies in this group. No study so far has shown any significant increase in iatrogenic hyperthermia from the use of these techniques. A high temperature on admission is usually secondary to a maternal fever.33
The most effective mode of transport within a hospital depends on the local configuration. Newly designed neonatal units are closely linked to the delivery suite to prevent the need for transport over long distances. Comparison of the use of radiant heaters with transport incubators for transfer has not shown any difference in admission temperatures.34 Transfer between units is most commonly done by ambulance. Heat loss is minimised by the use of double-walled incubators, heated gel mattresses, which warm patients through release of latent heat of crystallisation35 and plastic bags. Evaporative heat losses from the respiratory tract are reduced when ventilator gases are heated and humidified.
Ongoing care in the neonatal unit
As cold stress soon after delivery is associated with increased mortality there is no reason to assume that it is of any less importance during the immature baby's ongoing transition during the early days of life. Beyond the period of initial illness, failure to maintain an adequate thermal environment may increase apnoeic episodes36 and have an adverse effect on growth.37
The preterm baby, even if well, may be unable to maintain an adequate temperature without some additional source of heat. There is a variety of ways of achieving this including incubators, radiant heaters and heated mattresses. The heated gel or water-filled mattress is very effective in helping maintain the temperature of the well preterm baby while allowing easy access for the parents and staff. Clothes act as a significant thermal barrier to heat loss. Skin-to-skin contact is an effective way of maintaining body temperature, even in very preterm infants.38
Evaporative fluid and heat losses remain a challenge in the management of the preterm baby. The more immature the baby the higher the TEWL; subsequent evaporation is a major cause of fluid and heat loss. The skin matures rapidly after birth and in practical terms babies reach close to adult water losses from the skin at approximately 10–14 days of life.3 4
Evaporative water loss from the skin depends on the ambient water vapour pressure, irrespective of how the baby is being nursed. Various measures have been used to try and reduce these losses, with the most effective being an increase in the levels of humidity in the immediate environment of the baby. Careful attention to maintaining skin integrity will reduce ongoing transepidermal fluid losses. Preventing damage to the skin, for example from tape, is important. The use of semipermeable non-adhesive dressings lowers TEWL and reduces the bacteria numbers in the covered skin, but no study has shown any effect on fluid requirements.8 Emollients on the skin will prevent fluid loss and reduce drying, skin cracking and fissuring.9 They do not cause burns when exposed to radiant heat or phototherapy. A Cochrane review39 indicated that there is an increased risk of sepsis with the use of emollients, but studies conducted in low-resource countries suggest that their use can significantly reduce mortality.40
Control of the thermal environment is important for all babies, but it is the unwell, immature baby that presents the greatest challenge. They are usually nursed either in an incubator or on an open platform, under a radiant heater. A Cochrane review concluded that no study has shown any significant difference in outcome for babies nursed using either of these devices.41
The incubator provides a warm environment with heated air being circulated by a fan.
The heater output can be controlled in two ways. In air mode the incubator air temperature is set and the heater is thermostatically controlled to reach and maintain the set temperature. In servo mode a probe is taped to the infant and the desired skin temperature is set—the heater output varies to provide an air temperature that maintains the set skin temperature. In practice, air mode control is simpler to use, is safer and results in a very constant ambient air temperature regardless of the condition of the infant and the amount of care being received. Servo control results in wide fluctuations in air temperature, particularly during handling, and in the preterm baby this has been associated with an increase in apnoea and possibly a poorer outcome.36 The probe can become detached or wet, and the infant's own attempts at thermoregulation are overridden so that a fever may be disguised.
Heat loss by radiation to the cooler incubator walls is minimised by raising the temperature of the nursery and therefore of the incubator wall, by raising the incubator air temperature, with the use of a radiant heat shield within the incubator or by using a double-walled incubator. Evaporative losses are prevented by raising the humidity within the incubator. High humidity can cause ‘rain out’ on the inside of the canopy due to water condensing on the cold walls. This can be minimised by ensuring an adequate environmental temperature within the nursery (approximately 28°C).
The optimum time to make the transition from incubator to cot is unknown but most babies weighing between 1700 g and 1800 g are able to maintain their temperature, and continue to gain weight, when nursed clothed in a cot.
The infant lies naked on a platform with a radiant heat source above. The output of the heater is controlled by a temperature sensor on the infant's chest or abdomen with a set skin temperature of 36.5°C. The sensor should be shielded from the heat source.
Under a radiant heater there is high loss of fluid because of the low ambient water vapour pressure and not any direct effect of non-ionising radiation on the skin, but the temperature of the baby is maintained because of radiant heat gain. Wide fluctuations in heater output occur, producing a very uneven, asymmetrical thermal environment compared with an incubator. A plastic canopy over the baby can be used to create a humidified micro-environment. Warm humidified air can be passed under the shield or blanket but care must be taken to control the temperature and to make sure it does not affect the skin servo probe attached to the baby. If the cover is removed the humidity falls rapidly and the baby starts to lose large amounts of fluid. The radiant heater will compensate for any fall in the baby's temperature but fluid losses are a major concern.
Overheating can occur and regular measurement of the infant's body temperature by an independent method is essential. It is important to be sure that the skin temperature probe is securely attached to the baby. If the heater is switched off, moved to one side or if something is interposed between the infant and the heat source, the infant's heat losses are very great and rapid cooling occurs.
Babies nursed with similar skin temperatures have a higher basal metabolic rate when managed under radiant heaters compared with incubators.42 However, no study has shown any significant difference in outcome for babies nursed using either device.
New designs try to utilise the advantages of incubators and radiant heaters in a single device. During the change between the two modes there may be major fluctuations in the thermal environment but there are no comparative studies with other warming devices.
Ongoing improvements in outcome for the preterm baby will depend on an increasingly obsessional approach to all aspects of routine neonatal care, of which temperature control remains important. The goals are quite straightforward, maintaining a normal temperature and avoiding thermal stress, but the options to achieve the desired outcomes are varied, with little evidence to help in deciding the best device to use. Evaporative fluid and heat losses are of major importance and need to be controlled. Good temperature measurement is essential, particularly in the sick baby in whom dual temperatures should be continuously monitored and displayed.
Future designs should look to produce a single warming device that maintains a stable thermal environment and can be used throughout the care of the baby from birth to discharge home. Audit of temperature on admission and during transport should be done as measures of quality of care during vulnerable periods.
Competing interests None.
Provenance and peer review Commissioned; externally peer reviewed.