- Email: [email protected]
Applied physiology: temperature control in the newborn infant
ARTICLE IN PRESS Current Paediatrics (2004) 14, 137–144
www.elsevierhealth.com/journals/cuoe
Applied physiology: temperature control in the newborn infant Andrew Lyon* Simpson Centre for Reproductive Health, Royal Infirmary of Edinburgh, Little France, Edinburgh EH16 4SA, UK
KEYWORDS Newborn; Preterm; Temperature control; Humidity; Transepidermal water loss; Central–peripheral temperature difference
Summary It has been known for centuries that warmth is important for the newborn and in the 1950s randomised controlled trials showed that keeping babies warm significantly reduced neonatal mortality. Technology has improved our ability to keep even the most immature baby warm, but there is evidence that infants still become cold during resuscitation and that most units are not achieving the BAPM/RCPCH standard of an admission temperature of at least 361C. A low temperature on admission has been independently associated with an increased mortality in the preterm infant. Preventing evaporation, with the use of a plastic bag, while the baby is on the resuscitaire can abolish hypothermia on admission. There are no studies that show any difference in outcome for preterm babies nursed in incubators compared to those under radiant heaters. Care must be taken to reduce the very high transepidermal water losses under radiant heaters. The way a baby interacts with its environment is always changing and, whatever temperature and humidity settings are first used, it is necessary to monitor continuously the thermal balance. The continuous measurement and display of a central and a peripheral temperature gives an early indication of cold stress before there is any fall in the baby’s core temperature. & 2003 Elsevier Ltd. All rights reserved.
Practice points *
*
*
*
*
Hypothermia in the newborn infant is associated with adverse outcome Despite improvements in technology, the preterm baby is still at high risk of hypothermia immediately after delivery Prevention of evaporative heat losses eliminates hypothermia at resuscitation High evaporative fluid losses must be prevented if nursed under a radiant heater Continuous monitoring and display of the central and peripheral temperatures gives early warning of developing cold stress
*Tel.: þ 44(0)-131-242-2572. E-mail address: [email protected] (A. Lyon).
Introduction and historical perspective Soranus of Ephesus (98–138 AD), in his treatise ‘On Diseases on Women’, clearly understood the importance of keeping newborn infants warm. In the late 19th century Tarnier, and his student Budin in Paris, developed incubators based on a warming chamber used for rearing poultry that they had seen in the zoo. They showed that by use of this incubator the mortality of infants weighing under 2000 g at birth could be dramatically reduced from 66% to 38%.1 Such was the success of this ‘new technology’ that Martin Couney, a student of Budin, was the first person to offer specialised care for premature infants in USA. He also toured exhibitions and fairs showing off preterm babies in their incubators.2
0957-5839/$ - see front matter & 2003 Elsevier Ltd. All rights reserved. doi:10.1016/j.cupe.2003.11.012
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These exhibits were seen by a constant stream of fascinated, paying visitors. Incubator design developed through the first half of the 20th century with the introduction of high temperature alarms and thermostatic control of air temperature. William Silverman in the 1950s and others conducted a series of randomised controlled trials which showed that keeping babies warm in incubators resulted in an absolute reduction in mortality rate of 25%, compared with that of the 1950s.3–5 In many studies there were significant numbers of babies weighing under 1000 g at birth and the improvement in survival was seen in all birthweight groups. No single cause of death was reduced and it is not possible to determine the mechanism of the protective effect of warmth from these studies. No other single change in practice has had such a dramatic effect on mortality of newborn babies. Despite understanding the importance of keeping babies warm, we still see cold newborns admitted from delivery suites and postnatal wards. Care is needed in the management of the newborn baby being nursed by his mother in modern air conditioned rooms. It is the immature, preterm baby who remains the major challenge in temperature control. Since Silverman’s work there have been major changes in the non-thermal aspects of care, but there is still evidence that allowing these immature infants to get cold adversely affects outcome.6,7 Control of temperature within neonatal units has improved over the years, but these vulnerable babies are still at high risk of serious cold stress immediately after delivery, during resuscitation. The EPICure study of a cohort of babies under 26 weeks gestation, delivered in UK, showed that low admission temperature remained an independent risk factor for neonatal death after adjustment for other known risks.8 Others have reported an association between low temperature at the time of admission and increased mortality in preterm infants, even when other factors, including condition at birth, were taken into account.9 The report of the CESDI Project 27/2810 showed that most units were not achieving the BAPM/ RCPCH standard11 of an admission temperature for preterm infants of at least 361C. Temperature on admission to the neonatal unit was below this standard in 73% of babies who died and in 59% of survivors. The importance of temperature on admission as a predictor of outcome is also highlighted by its inclusion in the recent update of the Clinical Risk Index for Babies (CRIB) score.12
A. Lyon
Allowing very immature babies to become cold after delivery has an adverse effect on outcome. From reviews of practice within the UK it is clear that we have not been good enough at maintaining adequate temperatures for this vulnerable group during resuscitation and transfer to the neonatal unit.
Temperature control during resuscitation A baby exchanges heat with its environment by conduction, radiation, convection and evaporation. The preterm baby is at high risk of heat loss because of a high surface area to volume ratio and increased transepidermal water loss. The normal surge in metabolic rate which occurs after birth is much reduced, limiting heat production. The development in the control of skin blood-flow is also delayed in the immature baby, reducing the ability to maintain heat by peripheral vasoconstriction.13 Evaporation is the major mechanism of heat loss during resuscitation and temperature on admission can be significantly improved if transepidermal water losses are reduced using occlusive dressings.14 Clean plastic bags are easier to use than occlusive dressings and are effective in preventing evaporative heat losses immediately after delivery. The baby can be slid into the bag, up to the neck, whilst still wet. The head is covered with a hat. No blankets are used, allowing radiant heat to warm the infant through the bag (Figs. 1 and 2). Clinical inspection and auscultation during resuscitation can be done through the bag and if vascular access is needed, a small hole can be cut in the plastic. The infant can then be transported to the neonatal unit while still in the bag, which is only removed once the baby is in a humidified environment. It has been our practice to transfer the baby on the resuscitaire but local geography will dictate the best way to transport the baby from delivery suite to neonatal unit. Use of the plastic bags in this way abolishes hypothermia (o ¼ 351C) during resuscitation in newborn infants under 29 weeks gestation. In our experience babies cared for in this manner have a mean admission temperature of 371C,15 and this has also been reported by others.16 Once on the unit, the baby should be kept in the bag until it is in a stable humidified environment. Lines can be placed by cutting small holes in the bag for pulling out a limb or the umbilical cord. Monitoring is a problem as access is needed to place electrodes on the body. However, it is possible to achieve this with minimal
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Subsequent thermal care
Figure 1 Baby being put into plastic bag on resuscitaire.
Figure 2 Ventilated baby in plastic bag on resuscitaire.
disturbance to the humidified atmosphere within the plastic bag. No recent studies have shown an improvement in outcome by preventing hypothermia at resuscitation. Such a study would need large numbers of babies and, from the weight of available evidence, it would not be ethical to allow a group of babies to become cold after delivery. It is good practice to aim for the current BAPM/RCPCH standard 11 of an admission temperature of at least 361C in all babies. Units should record the temperature on admission as an audit of the adequacy of their resuscitation process.
The full term newborn will maintain a normal temperature if nursed fully dressed in a cot in a warm room. Recommendations for optimum environmental conditions for nursing healthy infants in the newborn period have been published.17 Care is needed in the design of delivery suites and postnatal wards, as well as in nursing processes, to prevent iatrogenic hypothermia in the well full term baby who is undergoing adaptation to extrauterine life. The preterm baby, even if well, may be unable to maintain an adequate temperature without some additional heat source. There are a variety of ways to achieve 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. Newborn infants needing intensive or high dependency care are often nursed naked to allow close observation and easy access for examination and treatment. This significantly affects temperature control as the naked baby’s resistance to heat loss is three times less than that of a clothed, wrapped infant.18,19 If stable, the preterm baby can be kept warm using skin to skin (kangaroo) care.20 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. The early clinical trials of Silverman and others showed that the use of incubators to keep babies warm improved outcome. There have not been any controlled studies that show that radiant heaters are as clinically effective. Babies nursed with similar skin temperatures have a higher basal metabolic rate when managed under radiant heaters when compared with incubators.21 However, no study has shown any significant difference in outcome for babies nursed using either of these devices, although Meyer 22 did report a non-significant trend to better outcome in babies nursed under a radiant heater.
Heat exchange The major methods of heat exchange with the environment in these babies are radiation and evaporation. In incubators heat exchange by
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convection is important, while under radiant heaters convection currents can cause some cooling of the baby, unless draughts are reduced by using sides on the platform. Babies on heated mattresses gain heat by conduction. The preterm baby in an incubator will lose heat by radiation to the colder walls. This can be reduced by dressing the baby if this is possible. Modern incubator designs use double walls to reduce radiative heat losses by keeping the inner wall at a higher temperature. Any additional radiant heat source placed above the incubator will reduce radiative heat losses from the baby by increasing the temperature of the outer walls.23 When nursed on an open platform, heat is gained by radiation from the heater above the baby.
Transepidermal water loss Transepidermal water losses (TEWL) are high in the immature baby. At 26 weeks gestation, on day 1 of life, the baby can lose over 50 kcal/kg via evaporation, compared with less than 5 kcal/kg in the term infant.24 Data from Hammerlund 24 suggest that the skin matures rapidly after birth and adult losses are reached at the age of around 10 days old in all babies. After this time the major source of heat loss in all babies is from radiation. More recently others have shown that in the very immature baby the maturation of the skin may take longer, and 30 weeks corrected age is a better estimate of the time taken to reach adult TEWL.25 In practical terms the amount of transepidermal water loss after about 14 days is unlikely to remain a major problem. Evaporative water loss from the skin depends on the ambient water vapour pressure, irrespective of how the baby is being nursed. The high rate of evaporation during care under a radiant heater is due to the low ambient water vapour pressure and is not due to any direct effect of non-ionising radiation on the skin.26 TEWL results in both loss of heat and fluid. Under a radiant heater the temperature of the baby is maintained because of radiant heat gain, but the large fluid losses can be a serious problem. Various interventions can help reduce evaporative fluid losses, mainly from the skin but also from the respiratory tract.
A. Lyon
humidity within the canopy. The use of a relative humidity of 80% significantly reduces TEWL in even the most immature infant.24 It is our practice to maintain all infants of less than 30 weeks gestation in 80% relative humidity until 7 days of age. Then we slowly reduce the level of humidity before stopping at 10 days of age, unless the baby shows poor thermal stability during this time. Modern designs use a sealed water system to produce the humidity and thereby minimise concerns about infection in humidified incubators. When the incubator portholes are open the air temperature within the canopy is maintained, but there is a rapid fall in the level of humidity. The handling of babies within incubators has been shown to be associated with increased thermal stress 27 and in the very immature infant, this is probably caused by the fall in environmental humidity resulting in increased evaporative heat losses. Increasing the air temperature will compensate for the heat loss but incubators are relatively slow to respond to such changes. High humidity within the incubator can cause ‘rain out’ on the inside of the canopy. This is caused by water condensing on the cold walls and can be minimised by ensuring an adequate environmental temperature within the nursery (of around 281C).
Radiant heaters TEWL is the major problem in babies nursed under radiant heaters. A shield or plastic blanket can be used to cover the baby and 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 ensure that 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 concern.
Maintenance of skin integrity Damage to the fragile skin of the preterm baby occurs easily and results in a significant increase both in TEWL and the risk of infection. Maintaining skin integrity is very important and any adhesives on the skin should be kept to a minimum.
Incubators
Skin coverings
Within an incubator it is relatively easy to raise the ambient water vapour pressure by introducing
Transparent adhesive dressings on the skin reduce fluid loss but cause significant damage, making
ARTICLE IN PRESS Temperature control in the newborn infant
them impractical. They also reduce the rate of skin maturation and it is postulated that the transepidermal movement of water is essential for the accelerated maturation of the skin seen in these babies.28 Use of semipermeable non-adhesive dressings lowers TEWL and reduces the number of bacteria in the covered skin.29 In a randomised controlled trial using semipermeable membranes in infants o 1000 g, the covered skin was in better condition, but there were no significant differences in fluid requirements or electrolyte status.30 Emollients are used to cover the skin and prevent fluid loss. They have been shown to be safe and do not cause burns when exposed to radiant heat or phototherapy. Their use reduces excessive drying, skin cracking and fissuring. However, the effect of these products wears off after about 3 h, necessitating repeated application.31 Treated infants have better skin scores and there were no differences found in bacterial skin counts, fungal counts or colonisation patterns, or fluid requirements and electrolyte status.32
Ventilator humidity There can be high fluid and heat losses from the respiratory tract of the ventilated baby. It is important to use adequate humidification in all ventilator circuits. Phototherapy The effect of phototherapy on TEWL is variable. No change was found in a group of thermally stable infants,33 yet others have reported an increase in TEWL despite the skin temperature and relative humidity remaining stable.34 Rather than increasing fluid intake because phototherapy has been started, fluid balance should be individually monitored and adjusted if necessary. Modern phototherapy units produce little heat but there is still some increase in the temperature at the top of the incubator canopy. This will reduce radiative heat losses and the incubator air temperature may have to be reduced to prevent a rise in the baby’s temperature.
Transport The transport of the newborn baby and particularly the preterm infant, presents many challenges but temperature control can be very difficult. Although incubators are heated there is likely to be a high radiative heat loss, especially in cold weather. This can be reduced by covering the incubator and using blankets around the baby. Evaporative heat loss can
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be reduced by using a plastic bag. There will be very high evaporative losses from the respiratory tract if ventilator gases are not heated and humidified. Heated gel mattresses that can be used during transport are available, with the baby gaining heat by conduction. It is important that all units transporting babies collect data on temperature control during transport and use this to audit efficacy of the transport process.
Servo vs air mode control Servo control works by a feedback loop in which a measurement from the baby, in this case a skin temperature, alters the output from a piece of medical equipment, i.e., the heat from an incubator or radiant heater. For the feedback loop to function the temperature probe must be correctly attached to the baby at all times, and shielded from direct heat from any external heat sources. Radiant heaters always use servo control while incubators can also be used in air mode control, in which the staff alter the air temperature around the baby. The baby’s skin temperature has to fall before the servo control increases heat output. Radiant heaters have a very fast response time and any fall in the baby’s temperature will be minimal. Incubator response times are much slower and servo control results in a significant degree of cold stress to the baby.35 There is an increased incidence of apnoea during the rising cycle of cyclic changes in incubator temperature.36 A comparison of servo and air mode controls showed better survival for the babies nursed in the more stable air temperature.37 Proportional control systems were introduced to servo mode in an attempt to reduce wide swings in incubator temperature. However, in real life steady state conditions rarely exist and in the comparison of the two modes of control there were no differences quantitatively or qualitatively in the degree and depth of cycling seen in babies with on/ off or proportional controlled incubators.37 Air mode control results in a more stable thermal environment within the incubator, and in the preterm baby, is the method of choice. There is a need for good continuous temperature monitoring to ensure the baby is not exposed to thermal stress.
Temperature monitoring and its interpretation The concept of the neutral thermal environment, in which a baby uses the minimum amount of energy
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in order to maintain thermal stability, has proven useful in determining the optimum environmental temperature for nursing the newborn baby.38,39 The published data are old and do not include any allowance for added humidity. This makes them less useful in the care of the very immature baby. Computer programs exist that use basic principles to calculate the heat exchange of a baby and give recommendations for the optimum environmental humidity and temperature settings.40 The way a baby interacts with its environment is always changing and, whatever settings are first used, it is necessary to monitor continuously the thermal balance. Continuous measurement of oxygen consumption, to allow calculation of energy expenditure, is not practical and in normal day to day care we are left with using temperature monitoring as a means of assessing the thermal stability of the baby. The temperature within tissue is a reflection of its metabolic rate, with the brain having the highest rate. It is important to measure a temperature that is representative of deep body core temperature. The rectum should not be used as there is a significant risk of damage to the mucosa. Rectal temperature is unreliable and is affected by the depth of insertion of the thermometer, whether the baby has just passed a stool and by the temperature of the blood returning from the lower limbs. It is difficult to retain the probes in the same position to allow continuous monitoring of a rectal temperature. The temperature of the skin over the liver or in the axilla reflects central temperature. A more accurate measurement can be obtained by placing the probe between the scapulae and a nonconducting mattress. No tape is needed on the skin as the baby lies on the probe, holding it in place. This so called zero heat flux temperature has been
A. Lyon
shown to be similar to the central temperature as measured by an oesophageal probe.41 The measurement of a single temperature tells us how well the baby is maintaining that temperature, but nothing about how much energy is being used to achieve thermal balance. The continuous measurement and display of a central (abdominal, axilla or zero heat flux) and a peripheral (foot) temperature detects cold stress, with the peripheral temperature falling before the central measurement changes (Fig. 3). The preterm baby who appears to be comfortable in its environment will have a central temperature, measured from a skin probe, of 36.8–37.31C and a central–peripheral temperature difference of 0.5– 11C. An increasing central–peripheral temperature difference, particularly of above 21C, is usually due to cold stress, and occurs before any fall in central temperature.13 Hypovolaemic babies will vasoconstrict their peripheral circulation in an attempt to maintain blood pressure. This results in an increase in the central–peripheral temperature difference but, in such cases, there are usually other signs of hypovolaemia, such as rising heart-rate and falling blood pressure.13A high central temperature, particularly if unstable, along with a wide central– peripheral gap is seen in septic babies.42
Conclusions There is evidence that despite major advances in the care of newborns, we are at risk of forgetting lessons from the past. Temperature control in the most immature newborns, particularly during their period of adaptation to extrauterine life, is generally poor and allowing these vulnerable babies to cool is associated with an adverse outcome. Simple measures can prevent hypothermia following
Figure 3 Increasing central (top trace) and peripheral (bottom trace) temperature difference showing cold stress during handling, with slow recovery.
ARTICLE IN PRESS Temperature control in the newborn infant
delivery. If hypothermia at birth is associated with poor outcome there is no reason to believe that preventing thermal stress is any less important once the baby is in the neonatal unit. It is important that the risks and benefits associated with various methods of controlling the infant’s temperature are fully understood.
References 1. Cone TE. Perspectives in neonatology. In: Sith GF, Vidyasagar D, editors. Historical Review and Recent Advances in Neonatal and Perinatal Medicine. Mead Johnson Nutritional Division, 1983, p. 9–33. 2. Silverman WA. Incubator-baby side shows. Pediatrics 1979;18:367–70. 3. Silverman WA, Blanc WA. Effect of humidity on survival of newly born premature infants. Pediatrics 1957;20:477–87. 4. Silverman WA, Fertig JW, Berger AP. The influence of the thermal environment upon survival of newly born preterm infants. Pediatrics 1958;22:876–85. 5. Silverman WA, Agate FJ, Fertig JW. A sequential trial of the non-thermal effect of atmospheric humidity on survival of human infants of low birth weight. Pediatrics 1963;31: 710–24. 6. Hazan J, Maag U, Chessex P. Association between hypothermia and mortality rate of premature infantsFrevisited. Am J Obstet Gynecol 1991;164:111–2. 7. Blakelock RT, Harding JE, Kolbe A, Pease PW. Gastroschisis: can morbidity be avoided? Ped Surg Int 1997;12:276–82. 8. Costeloe K, Hennessy E, Gibson AT, Marlow N, Wilkinson AR, for the EPICure Study Group. The EPICure study: outcomes to discharge from hospital for infants born at the threshold of viability. Pediatrics 2000;196:659–71. 9. Lyon AJ, Oxley C. Temperature on admission to the neonatal unitFa risk factor or just a reflection of condition at birth? Rhodes: Pediatr Res 2001;49:287. 10. CESDI Project 27/28. www.cemach.org.uk/publications/ p2728/mainreport.pdf (Accessed 01.08.03). 11. BAPM and RCPCH. Development of audit measures and guidelines for good practice in the management of neonatal respiratory distress syndrome. Report of Joint Working Group of British Association of Perinatal Medicine and the Research Unit of Royal College of Physicians. Arch Dis Child 1992;67:1221–7. 12. Parry G, Tucker J, Tarnow-Mordi W, for the UK Neonatal Staffing Study Collaborative Group. CRIB II: an update of the clinical risk index for babies score. Lancet 2003; 361:1789–91. 13. Lyon AJ, Pikaar ME, Badger P, McIntosh N. Temperature control in infants less than 1000 g birthweight in the first 5 days of life. Arch Dis Child 1997;76:F47–F50. 14. Vohra S, Frent G, Campbell V, Abbott M, Whyte R. Effect of polyethylene occlusive skin wrapping on heat loss in very low birth weight infants at delivery: a randomized trial. J Pediatr 1999;134:547–51. 15. Lyon AJ, Stenson B. Cold comfort for babies. Arch Dis Child 2003, in press. 16. Bjo. rklund LJ, Hellstro. m-Westas L. Reducing heat loss at birth in very preterm infants. Pediatrics 2000;137:739–40. 17. Hey EN. The care of babies in incubators. In: Gairdner D, Hull D, editors. Recent advances in Paediatrics. 4th ed.. London: J & A Churchill; 1971. p. 171–216.
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18. Hey EN, Katz G, O’Connell B. The total thermal insulation of the newborn baby. J Physiol 1970;207:683–9. 19. Hey EN Temperature regulation in sick infants. In: Tinker J, Rapin M, editors. Care of the critically ill patient. Berlin: Springer, 1983, p. 1013–1029. 20. Bauer K, Uhrig C, Sperling P, Pasel K, Wieland C, Versmold HT. Body temperatures and oxygen consumption during skinto-skin (kangaroo) care in stable preterm infants weighting less than 1500 grams. J Pediatr 1997;130:240–4. 21. LeBlanc MH. Relative efficacy of an incubator and an open warmer in producing thermoneutrality for the small premature infant. Pediatrics 1982;69:439–45. 22. Meyer MP, Payton MJ, Salmon A, Hutchinson C, deKlerk A. A clinical comparison of radiant warmer and incubator care for preterm infants from birth to 1800 grms. Pediatrics 2001;108:395–401. 23. Sjo. rs G, Hammerlund K, Sedin G. Thermal balance in term and preterm newborn infants nursed in an incubator equipped with a radiant heat source. Acta Paediatr 1997;86:403–9. 24. Hammerlund K, Stro. mberg B, Sedin G. Heat loss from the skin of preterm and fullterm newborn infants during the first weeks after birth. Biol Neonate 1986;50:1–10. 25. Kalia YN, Nonata LB, Lund CH, Guy RH. Development of skin barrier function in premature infants. J Invest Dermatol 1998;111:320–6. 26. Kjartansson S, Arsan S, Hammarlund K, Sjo. rs G, Sedin G. Water loss from the skin of term and preterm infants nursed under a radiant heater. Pediatr Res 1995;37:233–8. 27. Mok Q, Bass CA, Ducker DA, McIntosh N. Temperature instability during nursing procedures in preterm neonates. Arch Dis Child 1991;66:783–6. 28. Hanley K, Jiand Y, Elias PM, Feingold KR, Williams ML. Acceleration of barrier ontogenesis in vitro through air exposure. Pediatr Res 1997;41:293–9. 29. Mancini AJ, Sookdeo-Drost S, Madison KC, Smoller BR, Lane AT. Semipermeable dressings improve epidermal barrier function in premature infants. Pediatr Res 1994;36:306–14. 30. Donahue ML, Phelps DL, Richter SE, Davis JM. A semipermeable skin dressing for extremely low birth weight infants. J Perinatol 1996;16:20–6. 31. Nopper AJ, Horii KA, Sookdeo-Drost S, Wang TH, Mancini AJ, Lane AT. Topical ointment therapy benefits premature infants. J Pediatr 1996;128:660–9. 32. Pabst RC, Starr KP, Qaiyumi S, Schwalbe RS, Gewold IH. The effect of application of aquaphor on skin condition, fluid requirements, and bacterial colonization in very low birth weight infants. J Perinatol 1999;19:278–83. 33. Kjartansson S, Hammarlund K, Sedin G. Insensible water loss from the skin during phototherapy in term and preterm infants. Acta Paediatr 1992;81:764–8. 34. Grunhagen DJ, de Boer MG, de Beaufort AJ, Walther FJ. Transepidermal water loss during halogen spotlight phototherapy in preterm infants. Pediatr Res 2002;51:402–5. 35. Ducker DA, Lyon AJ, Ross Russell R, Bass CA, McIntosh N. Incubator temperature control: effects on the very low birthweight infant. Arch Dis Child 1985;60:902–7. 36. Perlstein PH, Edwards NK, Sutherland JM. Apnea in premature infants and incubator air temperature changes. N Eng J Med 1970;282:461–6. 37. Perlstein PH, Edwards NK, Atherton HD, et al. Computer assisted newborn intensive care. Pediatrics 1996;57: 494–501. 38. Hey EN, Katz G. The optimum thermal environment for naked babies. Arch Dis Child 1970;45:328–34.
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39. Sauer PJJ, Dane HJ, Visser HKA. New standards for neutral thermal environment of healthy very low birthweight infants in week one of life. Arch Dis Child 1984;59:18–22. 40. Lyon AJ, Oxley C. HeatBalance, a computer program to determine optimum incubator air temperature and humidity. A comparison against nurse settings for infants less than 28 weeks gestation. Early Hum Dev 2001;62:33–41.
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41. Dollberg S, Xi Y, Donnelly MM. A non-invasive alternative to rectal thermometry for continuous measurement of core temperature in the piglet. Pediatr Res 1993;34: 512–7. 42. Messaritakis J, Anagnostakis DH, Katerelos C. Rectal-skin temperature difference in septicaemic newborn infants. Arch Dis Child 1990;65:380–2.
www.elsevierhealth.com/journals/cuoe
Applied physiology: temperature control in the newborn infant Andrew Lyon* Simpson Centre for Reproductive Health, Royal Infirmary of Edinburgh, Little France, Edinburgh EH16 4SA, UK
KEYWORDS Newborn; Preterm; Temperature control; Humidity; Transepidermal water loss; Central–peripheral temperature difference
Summary It has been known for centuries that warmth is important for the newborn and in the 1950s randomised controlled trials showed that keeping babies warm significantly reduced neonatal mortality. Technology has improved our ability to keep even the most immature baby warm, but there is evidence that infants still become cold during resuscitation and that most units are not achieving the BAPM/RCPCH standard of an admission temperature of at least 361C. A low temperature on admission has been independently associated with an increased mortality in the preterm infant. Preventing evaporation, with the use of a plastic bag, while the baby is on the resuscitaire can abolish hypothermia on admission. There are no studies that show any difference in outcome for preterm babies nursed in incubators compared to those under radiant heaters. Care must be taken to reduce the very high transepidermal water losses under radiant heaters. The way a baby interacts with its environment is always changing and, whatever temperature and humidity settings are first used, it is necessary to monitor continuously the thermal balance. The continuous measurement and display of a central and a peripheral temperature gives an early indication of cold stress before there is any fall in the baby’s core temperature. & 2003 Elsevier Ltd. All rights reserved.
Practice points *
*
*
*
*
Hypothermia in the newborn infant is associated with adverse outcome Despite improvements in technology, the preterm baby is still at high risk of hypothermia immediately after delivery Prevention of evaporative heat losses eliminates hypothermia at resuscitation High evaporative fluid losses must be prevented if nursed under a radiant heater Continuous monitoring and display of the central and peripheral temperatures gives early warning of developing cold stress
*Tel.: þ 44(0)-131-242-2572. E-mail address: [email protected] (A. Lyon).
Introduction and historical perspective Soranus of Ephesus (98–138 AD), in his treatise ‘On Diseases on Women’, clearly understood the importance of keeping newborn infants warm. In the late 19th century Tarnier, and his student Budin in Paris, developed incubators based on a warming chamber used for rearing poultry that they had seen in the zoo. They showed that by use of this incubator the mortality of infants weighing under 2000 g at birth could be dramatically reduced from 66% to 38%.1 Such was the success of this ‘new technology’ that Martin Couney, a student of Budin, was the first person to offer specialised care for premature infants in USA. He also toured exhibitions and fairs showing off preterm babies in their incubators.2
0957-5839/$ - see front matter & 2003 Elsevier Ltd. All rights reserved. doi:10.1016/j.cupe.2003.11.012
ARTICLE IN PRESS 138
These exhibits were seen by a constant stream of fascinated, paying visitors. Incubator design developed through the first half of the 20th century with the introduction of high temperature alarms and thermostatic control of air temperature. William Silverman in the 1950s and others conducted a series of randomised controlled trials which showed that keeping babies warm in incubators resulted in an absolute reduction in mortality rate of 25%, compared with that of the 1950s.3–5 In many studies there were significant numbers of babies weighing under 1000 g at birth and the improvement in survival was seen in all birthweight groups. No single cause of death was reduced and it is not possible to determine the mechanism of the protective effect of warmth from these studies. No other single change in practice has had such a dramatic effect on mortality of newborn babies. Despite understanding the importance of keeping babies warm, we still see cold newborns admitted from delivery suites and postnatal wards. Care is needed in the management of the newborn baby being nursed by his mother in modern air conditioned rooms. It is the immature, preterm baby who remains the major challenge in temperature control. Since Silverman’s work there have been major changes in the non-thermal aspects of care, but there is still evidence that allowing these immature infants to get cold adversely affects outcome.6,7 Control of temperature within neonatal units has improved over the years, but these vulnerable babies are still at high risk of serious cold stress immediately after delivery, during resuscitation. The EPICure study of a cohort of babies under 26 weeks gestation, delivered in UK, showed that low admission temperature remained an independent risk factor for neonatal death after adjustment for other known risks.8 Others have reported an association between low temperature at the time of admission and increased mortality in preterm infants, even when other factors, including condition at birth, were taken into account.9 The report of the CESDI Project 27/2810 showed that most units were not achieving the BAPM/ RCPCH standard11 of an admission temperature for preterm infants of at least 361C. Temperature on admission to the neonatal unit was below this standard in 73% of babies who died and in 59% of survivors. The importance of temperature on admission as a predictor of outcome is also highlighted by its inclusion in the recent update of the Clinical Risk Index for Babies (CRIB) score.12
A. Lyon
Allowing very immature babies to become cold after delivery has an adverse effect on outcome. From reviews of practice within the UK it is clear that we have not been good enough at maintaining adequate temperatures for this vulnerable group during resuscitation and transfer to the neonatal unit.
Temperature control during resuscitation A baby exchanges heat with its environment by conduction, radiation, convection and evaporation. The preterm baby is at high risk of heat loss because of a high surface area to volume ratio and increased transepidermal water loss. The normal surge in metabolic rate which occurs after birth is much reduced, limiting heat production. The development in the control of skin blood-flow is also delayed in the immature baby, reducing the ability to maintain heat by peripheral vasoconstriction.13 Evaporation is the major mechanism of heat loss during resuscitation and temperature on admission can be significantly improved if transepidermal water losses are reduced using occlusive dressings.14 Clean plastic bags are easier to use than occlusive dressings and are effective in preventing evaporative heat losses immediately after delivery. The baby can be slid into the bag, up to the neck, whilst still wet. The head is covered with a hat. No blankets are used, allowing radiant heat to warm the infant through the bag (Figs. 1 and 2). Clinical inspection and auscultation during resuscitation can be done through the bag and if vascular access is needed, a small hole can be cut in the plastic. The infant can then be transported to the neonatal unit while still in the bag, which is only removed once the baby is in a humidified environment. It has been our practice to transfer the baby on the resuscitaire but local geography will dictate the best way to transport the baby from delivery suite to neonatal unit. Use of the plastic bags in this way abolishes hypothermia (o ¼ 351C) during resuscitation in newborn infants under 29 weeks gestation. In our experience babies cared for in this manner have a mean admission temperature of 371C,15 and this has also been reported by others.16 Once on the unit, the baby should be kept in the bag until it is in a stable humidified environment. Lines can be placed by cutting small holes in the bag for pulling out a limb or the umbilical cord. Monitoring is a problem as access is needed to place electrodes on the body. However, it is possible to achieve this with minimal
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Subsequent thermal care
Figure 1 Baby being put into plastic bag on resuscitaire.
Figure 2 Ventilated baby in plastic bag on resuscitaire.
disturbance to the humidified atmosphere within the plastic bag. No recent studies have shown an improvement in outcome by preventing hypothermia at resuscitation. Such a study would need large numbers of babies and, from the weight of available evidence, it would not be ethical to allow a group of babies to become cold after delivery. It is good practice to aim for the current BAPM/RCPCH standard 11 of an admission temperature of at least 361C in all babies. Units should record the temperature on admission as an audit of the adequacy of their resuscitation process.
The full term newborn will maintain a normal temperature if nursed fully dressed in a cot in a warm room. Recommendations for optimum environmental conditions for nursing healthy infants in the newborn period have been published.17 Care is needed in the design of delivery suites and postnatal wards, as well as in nursing processes, to prevent iatrogenic hypothermia in the well full term baby who is undergoing adaptation to extrauterine life. The preterm baby, even if well, may be unable to maintain an adequate temperature without some additional heat source. There are a variety of ways to achieve 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. Newborn infants needing intensive or high dependency care are often nursed naked to allow close observation and easy access for examination and treatment. This significantly affects temperature control as the naked baby’s resistance to heat loss is three times less than that of a clothed, wrapped infant.18,19 If stable, the preterm baby can be kept warm using skin to skin (kangaroo) care.20 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. The early clinical trials of Silverman and others showed that the use of incubators to keep babies warm improved outcome. There have not been any controlled studies that show that radiant heaters are as clinically effective. Babies nursed with similar skin temperatures have a higher basal metabolic rate when managed under radiant heaters when compared with incubators.21 However, no study has shown any significant difference in outcome for babies nursed using either of these devices, although Meyer 22 did report a non-significant trend to better outcome in babies nursed under a radiant heater.
Heat exchange The major methods of heat exchange with the environment in these babies are radiation and evaporation. In incubators heat exchange by
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convection is important, while under radiant heaters convection currents can cause some cooling of the baby, unless draughts are reduced by using sides on the platform. Babies on heated mattresses gain heat by conduction. The preterm baby in an incubator will lose heat by radiation to the colder walls. This can be reduced by dressing the baby if this is possible. Modern incubator designs use double walls to reduce radiative heat losses by keeping the inner wall at a higher temperature. Any additional radiant heat source placed above the incubator will reduce radiative heat losses from the baby by increasing the temperature of the outer walls.23 When nursed on an open platform, heat is gained by radiation from the heater above the baby.
Transepidermal water loss Transepidermal water losses (TEWL) are high in the immature baby. At 26 weeks gestation, on day 1 of life, the baby can lose over 50 kcal/kg via evaporation, compared with less than 5 kcal/kg in the term infant.24 Data from Hammerlund 24 suggest that the skin matures rapidly after birth and adult losses are reached at the age of around 10 days old in all babies. After this time the major source of heat loss in all babies is from radiation. More recently others have shown that in the very immature baby the maturation of the skin may take longer, and 30 weeks corrected age is a better estimate of the time taken to reach adult TEWL.25 In practical terms the amount of transepidermal water loss after about 14 days is unlikely to remain a major problem. Evaporative water loss from the skin depends on the ambient water vapour pressure, irrespective of how the baby is being nursed. The high rate of evaporation during care under a radiant heater is due to the low ambient water vapour pressure and is not due to any direct effect of non-ionising radiation on the skin.26 TEWL results in both loss of heat and fluid. Under a radiant heater the temperature of the baby is maintained because of radiant heat gain, but the large fluid losses can be a serious problem. Various interventions can help reduce evaporative fluid losses, mainly from the skin but also from the respiratory tract.
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humidity within the canopy. The use of a relative humidity of 80% significantly reduces TEWL in even the most immature infant.24 It is our practice to maintain all infants of less than 30 weeks gestation in 80% relative humidity until 7 days of age. Then we slowly reduce the level of humidity before stopping at 10 days of age, unless the baby shows poor thermal stability during this time. Modern designs use a sealed water system to produce the humidity and thereby minimise concerns about infection in humidified incubators. When the incubator portholes are open the air temperature within the canopy is maintained, but there is a rapid fall in the level of humidity. The handling of babies within incubators has been shown to be associated with increased thermal stress 27 and in the very immature infant, this is probably caused by the fall in environmental humidity resulting in increased evaporative heat losses. Increasing the air temperature will compensate for the heat loss but incubators are relatively slow to respond to such changes. High humidity within the incubator can cause ‘rain out’ on the inside of the canopy. This is caused by water condensing on the cold walls and can be minimised by ensuring an adequate environmental temperature within the nursery (of around 281C).
Radiant heaters TEWL is the major problem in babies nursed under radiant heaters. A shield or plastic blanket can be used to cover the baby and 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 ensure that 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 concern.
Maintenance of skin integrity Damage to the fragile skin of the preterm baby occurs easily and results in a significant increase both in TEWL and the risk of infection. Maintaining skin integrity is very important and any adhesives on the skin should be kept to a minimum.
Incubators
Skin coverings
Within an incubator it is relatively easy to raise the ambient water vapour pressure by introducing
Transparent adhesive dressings on the skin reduce fluid loss but cause significant damage, making
ARTICLE IN PRESS Temperature control in the newborn infant
them impractical. They also reduce the rate of skin maturation and it is postulated that the transepidermal movement of water is essential for the accelerated maturation of the skin seen in these babies.28 Use of semipermeable non-adhesive dressings lowers TEWL and reduces the number of bacteria in the covered skin.29 In a randomised controlled trial using semipermeable membranes in infants o 1000 g, the covered skin was in better condition, but there were no significant differences in fluid requirements or electrolyte status.30 Emollients are used to cover the skin and prevent fluid loss. They have been shown to be safe and do not cause burns when exposed to radiant heat or phototherapy. Their use reduces excessive drying, skin cracking and fissuring. However, the effect of these products wears off after about 3 h, necessitating repeated application.31 Treated infants have better skin scores and there were no differences found in bacterial skin counts, fungal counts or colonisation patterns, or fluid requirements and electrolyte status.32
Ventilator humidity There can be high fluid and heat losses from the respiratory tract of the ventilated baby. It is important to use adequate humidification in all ventilator circuits. Phototherapy The effect of phototherapy on TEWL is variable. No change was found in a group of thermally stable infants,33 yet others have reported an increase in TEWL despite the skin temperature and relative humidity remaining stable.34 Rather than increasing fluid intake because phototherapy has been started, fluid balance should be individually monitored and adjusted if necessary. Modern phototherapy units produce little heat but there is still some increase in the temperature at the top of the incubator canopy. This will reduce radiative heat losses and the incubator air temperature may have to be reduced to prevent a rise in the baby’s temperature.
Transport The transport of the newborn baby and particularly the preterm infant, presents many challenges but temperature control can be very difficult. Although incubators are heated there is likely to be a high radiative heat loss, especially in cold weather. This can be reduced by covering the incubator and using blankets around the baby. Evaporative heat loss can
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be reduced by using a plastic bag. There will be very high evaporative losses from the respiratory tract if ventilator gases are not heated and humidified. Heated gel mattresses that can be used during transport are available, with the baby gaining heat by conduction. It is important that all units transporting babies collect data on temperature control during transport and use this to audit efficacy of the transport process.
Servo vs air mode control Servo control works by a feedback loop in which a measurement from the baby, in this case a skin temperature, alters the output from a piece of medical equipment, i.e., the heat from an incubator or radiant heater. For the feedback loop to function the temperature probe must be correctly attached to the baby at all times, and shielded from direct heat from any external heat sources. Radiant heaters always use servo control while incubators can also be used in air mode control, in which the staff alter the air temperature around the baby. The baby’s skin temperature has to fall before the servo control increases heat output. Radiant heaters have a very fast response time and any fall in the baby’s temperature will be minimal. Incubator response times are much slower and servo control results in a significant degree of cold stress to the baby.35 There is an increased incidence of apnoea during the rising cycle of cyclic changes in incubator temperature.36 A comparison of servo and air mode controls showed better survival for the babies nursed in the more stable air temperature.37 Proportional control systems were introduced to servo mode in an attempt to reduce wide swings in incubator temperature. However, in real life steady state conditions rarely exist and in the comparison of the two modes of control there were no differences quantitatively or qualitatively in the degree and depth of cycling seen in babies with on/ off or proportional controlled incubators.37 Air mode control results in a more stable thermal environment within the incubator, and in the preterm baby, is the method of choice. There is a need for good continuous temperature monitoring to ensure the baby is not exposed to thermal stress.
Temperature monitoring and its interpretation The concept of the neutral thermal environment, in which a baby uses the minimum amount of energy
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in order to maintain thermal stability, has proven useful in determining the optimum environmental temperature for nursing the newborn baby.38,39 The published data are old and do not include any allowance for added humidity. This makes them less useful in the care of the very immature baby. Computer programs exist that use basic principles to calculate the heat exchange of a baby and give recommendations for the optimum environmental humidity and temperature settings.40 The way a baby interacts with its environment is always changing and, whatever settings are first used, it is necessary to monitor continuously the thermal balance. Continuous measurement of oxygen consumption, to allow calculation of energy expenditure, is not practical and in normal day to day care we are left with using temperature monitoring as a means of assessing the thermal stability of the baby. The temperature within tissue is a reflection of its metabolic rate, with the brain having the highest rate. It is important to measure a temperature that is representative of deep body core temperature. The rectum should not be used as there is a significant risk of damage to the mucosa. Rectal temperature is unreliable and is affected by the depth of insertion of the thermometer, whether the baby has just passed a stool and by the temperature of the blood returning from the lower limbs. It is difficult to retain the probes in the same position to allow continuous monitoring of a rectal temperature. The temperature of the skin over the liver or in the axilla reflects central temperature. A more accurate measurement can be obtained by placing the probe between the scapulae and a nonconducting mattress. No tape is needed on the skin as the baby lies on the probe, holding it in place. This so called zero heat flux temperature has been
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shown to be similar to the central temperature as measured by an oesophageal probe.41 The measurement of a single temperature tells us how well the baby is maintaining that temperature, but nothing about how much energy is being used to achieve thermal balance. The continuous measurement and display of a central (abdominal, axilla or zero heat flux) and a peripheral (foot) temperature detects cold stress, with the peripheral temperature falling before the central measurement changes (Fig. 3). The preterm baby who appears to be comfortable in its environment will have a central temperature, measured from a skin probe, of 36.8–37.31C and a central–peripheral temperature difference of 0.5– 11C. An increasing central–peripheral temperature difference, particularly of above 21C, is usually due to cold stress, and occurs before any fall in central temperature.13 Hypovolaemic babies will vasoconstrict their peripheral circulation in an attempt to maintain blood pressure. This results in an increase in the central–peripheral temperature difference but, in such cases, there are usually other signs of hypovolaemia, such as rising heart-rate and falling blood pressure.13A high central temperature, particularly if unstable, along with a wide central– peripheral gap is seen in septic babies.42
Conclusions There is evidence that despite major advances in the care of newborns, we are at risk of forgetting lessons from the past. Temperature control in the most immature newborns, particularly during their period of adaptation to extrauterine life, is generally poor and allowing these vulnerable babies to cool is associated with an adverse outcome. Simple measures can prevent hypothermia following
Figure 3 Increasing central (top trace) and peripheral (bottom trace) temperature difference showing cold stress during handling, with slow recovery.
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delivery. If hypothermia at birth is associated with poor outcome there is no reason to believe that preventing thermal stress is any less important once the baby is in the neonatal unit. It is important that the risks and benefits associated with various methods of controlling the infant’s temperature are fully understood.
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18. Hey EN, Katz G, O’Connell B. The total thermal insulation of the newborn baby. J Physiol 1970;207:683–9. 19. Hey EN Temperature regulation in sick infants. In: Tinker J, Rapin M, editors. Care of the critically ill patient. Berlin: Springer, 1983, p. 1013–1029. 20. Bauer K, Uhrig C, Sperling P, Pasel K, Wieland C, Versmold HT. Body temperatures and oxygen consumption during skinto-skin (kangaroo) care in stable preterm infants weighting less than 1500 grams. J Pediatr 1997;130:240–4. 21. LeBlanc MH. Relative efficacy of an incubator and an open warmer in producing thermoneutrality for the small premature infant. Pediatrics 1982;69:439–45. 22. Meyer MP, Payton MJ, Salmon A, Hutchinson C, deKlerk A. A clinical comparison of radiant warmer and incubator care for preterm infants from birth to 1800 grms. Pediatrics 2001;108:395–401. 23. Sjo. rs G, Hammerlund K, Sedin G. Thermal balance in term and preterm newborn infants nursed in an incubator equipped with a radiant heat source. Acta Paediatr 1997;86:403–9. 24. Hammerlund K, Stro. mberg B, Sedin G. Heat loss from the skin of preterm and fullterm newborn infants during the first weeks after birth. Biol Neonate 1986;50:1–10. 25. Kalia YN, Nonata LB, Lund CH, Guy RH. Development of skin barrier function in premature infants. J Invest Dermatol 1998;111:320–6. 26. Kjartansson S, Arsan S, Hammarlund K, Sjo. rs G, Sedin G. Water loss from the skin of term and preterm infants nursed under a radiant heater. Pediatr Res 1995;37:233–8. 27. Mok Q, Bass CA, Ducker DA, McIntosh N. Temperature instability during nursing procedures in preterm neonates. Arch Dis Child 1991;66:783–6. 28. Hanley K, Jiand Y, Elias PM, Feingold KR, Williams ML. Acceleration of barrier ontogenesis in vitro through air exposure. Pediatr Res 1997;41:293–9. 29. Mancini AJ, Sookdeo-Drost S, Madison KC, Smoller BR, Lane AT. Semipermeable dressings improve epidermal barrier function in premature infants. Pediatr Res 1994;36:306–14. 30. Donahue ML, Phelps DL, Richter SE, Davis JM. A semipermeable skin dressing for extremely low birth weight infants. J Perinatol 1996;16:20–6. 31. Nopper AJ, Horii KA, Sookdeo-Drost S, Wang TH, Mancini AJ, Lane AT. Topical ointment therapy benefits premature infants. J Pediatr 1996;128:660–9. 32. Pabst RC, Starr KP, Qaiyumi S, Schwalbe RS, Gewold IH. The effect of application of aquaphor on skin condition, fluid requirements, and bacterial colonization in very low birth weight infants. J Perinatol 1999;19:278–83. 33. Kjartansson S, Hammarlund K, Sedin G. Insensible water loss from the skin during phototherapy in term and preterm infants. Acta Paediatr 1992;81:764–8. 34. Grunhagen DJ, de Boer MG, de Beaufort AJ, Walther FJ. Transepidermal water loss during halogen spotlight phototherapy in preterm infants. Pediatr Res 2002;51:402–5. 35. Ducker DA, Lyon AJ, Ross Russell R, Bass CA, McIntosh N. Incubator temperature control: effects on the very low birthweight infant. Arch Dis Child 1985;60:902–7. 36. Perlstein PH, Edwards NK, Sutherland JM. Apnea in premature infants and incubator air temperature changes. N Eng J Med 1970;282:461–6. 37. Perlstein PH, Edwards NK, Atherton HD, et al. Computer assisted newborn intensive care. Pediatrics 1996;57: 494–501. 38. Hey EN, Katz G. The optimum thermal environment for naked babies. Arch Dis Child 1970;45:328–34.
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39. Sauer PJJ, Dane HJ, Visser HKA. New standards for neutral thermal environment of healthy very low birthweight infants in week one of life. Arch Dis Child 1984;59:18–22. 40. Lyon AJ, Oxley C. HeatBalance, a computer program to determine optimum incubator air temperature and humidity. A comparison against nurse settings for infants less than 28 weeks gestation. Early Hum Dev 2001;62:33–41.
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41. Dollberg S, Xi Y, Donnelly MM. A non-invasive alternative to rectal thermometry for continuous measurement of core temperature in the piglet. Pediatr Res 1993;34: 512–7. 42. Messaritakis J, Anagnostakis DH, Katerelos C. Rectal-skin temperature difference in septicaemic newborn infants. Arch Dis Child 1990;65:380–2.