CLINICAL ISSUES

Thermoregulation and Heat Loss Prevention After Birth and During Neonatal Intensive-Care Unit Stabilization of Extremely Low-Birthweight Infants
Robin Knobel and Diane Holditch-Davis

Extremely low-birthweight infants have inefcient thermoregulation due to immaturity and may exhibit cold body temperatures after birth and during their rst 12 hours of life. Hypothermia in these infants can lead to increased morbidity and mortality. Anecdotal notes made during our recent study revealed extremely low-birthweight infants temperatures decreased with caregiver procedures such as umbilical line insertion, intubations, obtaining chest x-rays, manipulating intravenous lines, repositioning, suctioning, and taking vital signs during the rst 12 hours of life. Therefore, nursing interventions should be undertaken to prevent heat loss during these caregiver procedures. Nurses can improve the thermal environment for extremely lowbirthweight infants by prewarming the delivery room and placing the infant in a plastic bag up to the neck during delivery room stabilization to prevent heat loss. JOGNN, 36, 280-287; 2007. DOI: 10.1111/J.15526909.2007.00149.x Keywords: Delivery room resuscitationELBW infantsHypothermiaNeonatal thermoregulation Accepted: November 2006

their care because hypothermia can lead to increased mortality and morbidity (Hazan, Maag, & Chessex, 1991; Vohra, Grent, Campbell, Abbott, & Whyte, 1999). This paper will review thermoregulation and cold stress in the ELBW infant, describe observational data from a study evaluating temperature in 10 ELBW infants during their rst 12 hours of life (Knobel, 2006), and suggest nursing interventions that may prevent heat loss in this vulnerable population.

Basics of Neonatal Thermoregulation

Human Thermoregulation
When exposed to a cold environment, infant body temperature decreases, and peripheral and central thermoreceptors detect change (Widmaier, Raff, & Strang, 2005). The thermoregulatory system of humans consists of these thermal sensors, afferent pathways, an integration system in the central nervous system, efferent pathways, and target organs that control heat generation and transfer (Nadel, 2003). Peripheral thermoreceptors sense the temperature on the skin. They are free nerve endings that are distributed over the entire skin surface (Nadel, 2003). They have the ability to detect warm or cold areas on the skin and send signals forward by way of afferent nerve bers that carry sensory information to the hypothalamic regulatory center (Widmaier et al., 2005). A change in the skins normal temperature causes the receptors to increase their ring rate from the steady-state rate (Nadel). Their signals also travel by thalamic pathways to the cerebral cortex, causing conscious perception of the thermal environment and resulting in behavioral adjustments (Nadel).

About 33,000 extremely low-birthweight (ELBW) infants (less than 1,000 g) were born in the United States in 2003, which is 0.8% of all infants born that year. Extremely low-birthweight infants typically have a gestational age less than 28 to 29 weeks. These infants accounted for almost 49% of all infant deaths in 2003 (Mathews & MacDorman, 2006). Because ELBW infants are so fragile, they need more specialized care in the neonatal intensive-care unit (NICU) than larger premature infants. Thermal control for these infants is an important aspect of 280 JOGNN

2007, AWHONN, the Association of Womens Health, Obstetric and Neonatal Nurses

Central thermoreceptors are located in deep body structures including the hypothalamus, spinal cord, and abdominal organs (Widmaier et al., 2005). These thermoreceptors are part of a negative feedback system, modifying heat transfer rates to restore core temperature to its regulated level once they detect the core temperature is colder or warmer than normal (Nadel, 2003). The preoptic and anterior nuclei of the hypothalamus receive signals from the peripheral and central thermoreceptors (Guyton & Hall, 2006). The hypothalamus, the primary integrator of hormonal and system responses, is the most important control area for homeostatic regulation and has pathways that form the master command center for neural and endocrine coordination. The hypothalamus monitors the prevailing thermal status and if not within a normal set of thermal conditions sends efferent signals to alter the rate of heat generation and heat transfer within and from the body (Nadel, 2003).

Infant Thermoregulation
In adults, the immediate responses to a cold body temperature are peripheral vasoconstriction to diminish heat loss, inhibition of sweating, and initiation of shivering, with a resultant increase in heat production. The effector mechanisms of skeletal muscle stimulation are minimal in infants, so infants do not shiver in response to a cold environment. Therefore, vasoconstriction is the main result of activation of peripheral skin receptors (Guyton & Hall, 2006). Nonshivering thermogenesis is the main mechanism in neonates to produce heat through metabolic activity (see Figure 1). Increased sympathetic activity, controlled in the hypothalamic ventromedial nucleus, causes norepinephrine to be released from nerve endings terminating on the surface of brown adipocytes (brown fat), while simultaneously causing an increase in thyroid-stimulating hormone. Thyroid-stimulating hormone stimulates the release of thyroid hormones, mostly thyroxine (T4), and norepinephrine

FIGURE 1

Physiology of nonshivering thermogenesis (metabolic heat production in the infant).

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activates 5/3-monodeiodinase, causing T4 to convert to triiodothyronine (T3) (Barrett, 2003). T3 generated in brown adipose tissue upregulates an uncoupling protein (UCP or thermogenin), thereby uncoupling mitochondrial oxidation from phosphorylation in the brown adipose tissue and causing heat production. In the presence of free fatty acids, thermogenin allows protons to enter the mitochondria and uncouples adenosine triphosphate (ATP) synthesis. As a result, the mitochondria in brown adipose tissue can produce heat without storing energy through ATP (Jones & DeCherney, 2003). Thermoregulation in the ELBW Infant. Nonshivering thermogenesis yields heat through oxidation of free fatty acids (Guyton & Hall, 2006; Widmaier et al., 2005) and depends on adequate components of heat production, mainly brown fat, 5/3-monodeiodinase, and thermogenin (Jones & DeCherney, 2003). Thermoregulation processes are inefcient in ELBW infants because of the infants immature organ systems and lower levels of thermogenin and 5/3-monodeiodinase (Houstek et al., 1993). Brown adipose tissue begins to develop as early as the 75-mm fetal stage (Hatai, 1902). Hull (1977) calculated that 20 to 30 g of brown adipose tissue are necessary to handle all the nonshivering thermogenesis needs of a newborn baby. The structure of brown adipose tissue is well developed in preterm infants at as early as 25 weeks gestational age (Sauer, 1995), with brown fat comprising about 1% to 2% of body weight (Nechad, 1986). Brown adipose tissue is not the only factor essential for nonshivering thermogenesis. The level of thermogenin in infants increases from 29.4 3.3 pmol/mg at 25 weeks gestational age to 62.5 10.2 pmol/mg at 40 weeks (Houstek et al., 1993). A major increase in thermogenin occurs at 32 weeks gestational age, approximately the time when a neonate can use nonshivering thermogenesis to generate heat effectively. The enzyme 5/3-monodeiodinase is active at 25 weeks gestational age, shows a major increase in amount at 32 weeks gestational age (Houstek et al., 1993), and increases fourfold by term. Low levels of thermogenin and 5/3-monodeiodinase before 32 weeks are the probable causes of ineffective nonshivering thermogenesis in ELBW infants.

that defines hypothermia in ELBW infants has not been reported.

espite advanced technology, ELBW infants exhibit cold body temperatures after delivery room stabilization and throughout their rst 12 hours in the NICU.

Hypothermia and Cold Stress

Effects of Hypothermia
Hypothermia is abnormally low body temperature. In the 1980s, the American Academy of Pediatrics and the College of Obstetrics and Gynecologists (1988) defined hypothermia for larger infants as below 36.4C, but a temperature indicating hypothermia was not specified in later guidelines, and the body temperature 282 JOGNN

Despite advanced technology, ELBW infants continue to exhibit cold body temperatures after delivery room stabilization and throughout their rst 12 hours in the NICU. Approximately 66% to 93% of ELBW infants are admitted to NICUs with hypothermic temperatures (Knobel, Wimmer, & Holbert, 2005; Loughead, Loughead, & Reinhart, 1997). Horns (2002) found that 90% of an ELBW sample had extremely cold peripheral temperatures even when cared for in the controlled environment of an incubator. Thomas (2003) found preterm infants in incubators exhibited temperatures as low as 33.1C during caregiver interventions. Cold stress occurs when an exposed infant loses more heat than he or she can produce. The potential harms are signicant. In the 1950s to 1960s, when infants were deliberately exposed to colder temperatures, a procedure that would not be ethical today, exposure to cold was linked to increased mortality (Day, Caliguiri, Kamenski, & Ehrlich, 1964; Silverman, Fertig, & Berger, 1958). A variety of physiological processes contribute to this harmful effect. Infants oxygen consumption has been found to increase in response to hypothermia because of the energy demands of nonshivering thermogenesis (Malin & Baumgart, 1987). Although oxygen consumption has not been evaluated in ELBW infants because their tidal volumes are too low for accurate measurement, increased oxygen consumption can lead to acidosis and hypoglycemia in larger infants. Hypothermia may also lead to a fall in systemic arterial pressure, decreased plasma volume, decreased cardiac output, and increased peripheral resistance (Sinclair, 1992). If left unchecked, these conditions can lead to permanent tissue damage, brain damage, or death (Deshpande & Platt, 1997).

ELBW Infants Responses to Hypothermia

Extremely low-birthweight infants are at particular risk for cold stress. When an ELBW infant experiences heat loss, the physiological responses to heat loss create demands that exceed the infants normal physiological balance because energy will need to be expended and oxygen will be metabolized to produce heat. Before 30 weeks gestation, preterm infants have very little body fat and thin skin. They Volume 36, Number 3

typically rest with arms and legs extended, instead of being exed like term infants, exposing more of their body surface to the environment (Jones & DeCherney, 2003). Extremely low-birthweight infants also have poor vasomotor control at birth (Horns, 2002; Lyon et al., 1997) and are unlikely to exhibit peripheral vasoconstriction to conserve heat. Thus, ELBW infants are at greater risk than larger, more mature infants for heat loss and subsequent cold stress. Extremely low-birthweight infants are further stressed by physiological adaptations to extrauterine life that take place during these periods. The newborn infant must change from fetal circulation to neonatal circulation and from placental gas exchange to pulmonary gas exchange (Askin, 2002). The onset of neonatal breathing causes a drop in pulmonary vascular resistance (Mathew, 1998). Initial closure of the ductus arteriosus, which completes the switch to neonatal circulation, is a gradual process that occurs over the rst 10 to 15 hours after birth (Askin). These extrauterine adaptations may be more difcult for preterm infants because these infants may also have lung surfactant deciency, commonly called respiratory distress syndrome, altering ventilation and oxygenation (Askin).

1998). Consequently, the ELBW infant may become acidotic (Deshpande & Platt; Seri, 1998). Increased energy expenditure in an already sick and unstable infant can affect vital signs, pH balance, glucose balance, and oxygenation (see Figure 2). Decreased oxygenation, increased acidosis, decreased blood glucose, and increased heart rate due to cold stress can lead to increased morbidity and mortality (Richardson, Corcoran, Escobar, & Lee, 2001). Thus, thermoregulation continues to be one of the primary priorities of nursing care for ELBW infants.

Routes of Heat Loss in the Neonatal Period

Extremely low-birthweight infants lose heat during birth and stabilization in the delivery room, transfer to the NICU, and stabilization procedures in the NICU. Understanding the ways in which these infants lose heat from their bodies is important in order to develop nursing interventions to prevent cold stress. Human thermoregulation attempts to keep body temperature in a steady state, in which thermogenesis (heat production) equals heat loss. The rate of heat loss depends on how rapidly heat is transferred from the inner body to the skin and how fast heat can be transferred from the skin to the environment. The skin, along with subcutaneous tissues and fat, acts as an insulator for the body. Fat conducts heat only one third as readily as other body tissues (Guyton & Hall, 2006). Skin transfers heat to the environment by way of radiation, conduction, convection, and evaporation. Radiation is the process by which all body surfaces emit heat in the form of electromagnetic waves (Guyton & Hall, 2006; Nadel, 2003). The infrared portion of the electromagnetic energy spectrum, commonly known as heat, carries this energy. The rate of heat loss is proportional to the temperature difference between the skin and the radiating body. Heat may be lost from the infants body to a nearby

Inefcient Nonshivering Thermogenesis

Brown fat metabolism is inefcient in ELBW infants due to extreme immaturity (Houstek et al., 1993) and may not produce enough heat to prevent body temperature from falling. Because oxygen is needed to produce heat, oxygenation of the ELBW infant during cold stress may be decreased (Voet, Voet, & Pratt, 2002). Glucose is also consumed in thermogenesis, depleting ELBW infants minimal energy stores (Voet et al., 2002). As a result, lactic acid accumulates (Deshpande & Platt, 1997), and the cardiovascular system must work harder to increase cardiac output (Anderson, Kleinman, Lister, & Talner,

FIGURE 2

Proposed effect of decreased body temperature on oxygenation, acid-base balance, glucose balance, and heart rate in the ELBW infant. (NST = Nonshivering Thermogenesis)

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cold wall, or heat may be gained by the skin from a heat lamp near the infant. In infants older than 28 weeks gestational age, heat loss from radiation is the most important route of heat transfer from birth onward. Radiative heat losses are initially low in ELBW infants but gradually increase with age and become the most important route of heat transfer after the rst postnatal week (Sedin, 1995). Heat transfers by conduction occur when the skin is in contact with a surface of a different temperature (Guyton & Hall, 2006; Nadel, 2003). Heat moves from infant skin surface molecules to the molecules of another surface (air, water, or solid surface such as mattress) as they collide. In the NICU, conductive heat gain or loss is minimized by positioning infants on prewarmed surfaces. Heat is transferred by convection when moving air or water currents carry heat away from the body surface to the environment (Guyton & Hall, 2006; Nadel, 2003). Warm molecules rise into the air from the skin because molecules move from a higher temperature with higher energy to a lower temperature with lower energy. If the infants body surface is warmer than the surrounding air, heat is rst conducted into the air and then swept away by convective air currents. Convection is the source of heat loss when an infant is carried from the mother on the delivery room table through the cool air to the radiant warmer table. Heat loss by evaporation occurs when water is lost from the skin and membrane linings of the respiratory tract. During evaporation, water is converted from a liquid to a gas. The evaporative rate is proportional to the water vapor pressure gradient between the skin and the environment and is independent of the temperature gradient between the skin and the environment (Nadel, 2003). As the water vapor escapes into the air because of a vapor pressure gradient between the body surface and the air, heat is lost from the infant into the air. Evaporation causes 0.6 kcal of heat to be lost for every 1 g of water lost from the body (Guyton & Hall, 2006; Nadel). For infants 25 to 27 weeks gestational age in dry environments, evaporative heat loss is the major form of heat loss during the rst 10 days of life. Hammarlund and Sedin (1979) found that transepidermal water loss in infants was inversely correlated with gestational age, with infants born at 25 weeks gestational age losing 15 times more water than term infants, because more immature preterm infants have thinner skin. These high evaporative heat losses in preterm infants during the rst few hours and days of life gradually decrease with advancing postnatal age (Sedin, 1995), most likely because of skin maturation. If infants are kept in an environment with 60% humidity, evaporative heat loss is much lower (Sedin). A neutral thermal environment is the environmental condition in which the temperature of the naked body does not change when the subject is at rest and there is no muscle activity (Nadel, 2003). In a neutral thermal environment, the airow, humidity, and temperature of sur284 JOGNN

rounding radiating surfaces will minimize heat loss or gain through radiation, conduction, convection, and evaporation to keep the infant in a steady metabolic state.

Nursing Interventions to Prevent Heat Loss and Cold Stress

Plastic Bags in the Delivery Room
Cold stress is most likely immediately after birth, when the infant is delivered from the warm intrauterine environment to a cold drafty delivery room. The newborn infant is covered in amniotic uid; therefore, much heat is lost quickly by evaporation.

sing a plastic bag or wrap on ELBW infants immediately after birth increases NICU admission temperatures.

Researchers have found that using a plastic bag or wrap on ELBW infants immediately after birth increases NICU admission temperatures (Knobel, Wimmer, & Hobert, 2005; Vohra, Roberts, Zhang, Janes, & Schmidt, 2004; Vohra et al., 1999). A meta-analysis of three randomized controlled trials and ve historic controlled trials including a total of 998 infants showed that infants wrapped in plastic material (e.g., polyethylene, polyurethane) had signicantly higher admission temperatures than unwrapped infants, with mean temperatures of 36.0C to 37.0C in the wrapped groups versus 35.3C to 36.1C in the nonwrapped groups (Cramer, Wiebe, Hartling, Crumley, & Vohra, 2005). The American Academy of Pediatrics and American Heart Association (2005) now recommend that the use of polyethylene bags be considered to prevent heat loss in very low-birthweight infants (less than 1,500 g) during delivery room resuscitation. Prior to this recommendation, we found that only 20% of the 125 NICUs responding to a survey of 411 NICUs across the United States used this intervention (Knobel, Vohra, & Lehmann, 2005). As in our previous study (Knobel, Wimmer, et al., 2005), current protocol in our NICU includes use of polyurethane bags by DeRoyal, Powell, TN, USA (REF305010, sterile transportation bag 19 18) to prevent heat loss by evaporation in the delivery room. After the infant is delivered and placed on the warmer, he or she is immediately placed in a polyurethane bag up to the neck, while still covered with amniotic uid. The infants head is dried and covered by a hat. Resuscitation continues using Volume 36, Number 3

the standard neonatal resuscitation protocol. The infants heart rate can easily be auscultated through the bag with a stethoscope. The infant in the bag is transferred to the NICU, with warm blankets placed over the infants body on the warmer table with the heat turned off during transfer. Because our previous study (Knobel, Wimmer, et al., 2005) did not use a radiant heat source on the infant during transport to the NICU, care should be taken that the infant is not overheated if additional heat is used while the infant is in a bag.

Preparing and Maintaining a Warm Environment

Nurses need to prewarm the incubator or radiant warmer before the infant arrives in the NICU. A warm incubator or warmer will help prevent conductive and radiative heat loss. As admissions of ELBW infants are often not announced, a warm incubator should be available at all times for unexpected deliveries. Porthole covers for the incubator need to be in place prior to the infants arrival. Linens, clothing, and gel mattresses should be prewarmed before placing these items next to the infants skin. Although these interventions seem obvious, they can be forgotten for hours after the admission. The time required for procedures such as umbilical catheter insertion needs to be limited because heat cannot reach infant body surfaces while infants are under sterile drapes. This may be a particular problem in institutions that have rst- and second-year residents or nurse practitioner students because trainees may need extra time to insert umbilical lines. The nurse needs to keep track of procedure time and monitor the infants temperature. In addition, placing a warm transport gel mattress under the blanket during procedures may be benecial. Auxiliary heat lamps also may be used. The light will also help speed the catheter insertion process by better illuminating the umbilical area. Once the procedure is complete, the incubator top is closed as quickly as possible to allow convective heat to circulate around the infant. Humidity needs to be added as soon as the incubator top is closed and kept at 50% or greater (Sedin, 1995) to reduce evaporative heat loss. Infants in our study were cared for in closed Giraffe incubators with up to 80% humidity. Many times when the door of the incubator was opened or the humidity level decreased below about 60%, infant body temperatures decreased by as much as 1C within 5 minutes. Infant temperature quickly rebounded when humidity was increased. Ventilator heaters need to be set at a warm temperature before use. Previous research has not examined the optimal ventilator temperatures for ELBW infants. In the study of NICU, ventilator temperatures were controlled at approximately 35C to 38C. We observed infant temperatures decreased up to 1C when ventilator temperatures decreased to 29C to 34C. Such a decrease in ventilator temperature can occur when the heater is malfunctioning or the water has been depleted. Thus, care needs to be taken to insure the water in the ventilator heater does not run out. Intravenous uids need to be prewarmed by placing the syringe or bag of intravenous uid into the incubator before delivering the uid to the ELBW infant. In our study, infant abdominal temperature decreased when uid boluses were given through umbilical venous catheters. No previous research has documented temperature decreases in ELBW infants related to cold intravenous uid infusions. However, standard protocols for exchange transfusions, whereby an infants blood is removed slowly while JOGNN 285

Delivery Room Temperature

Delivery rooms are usually kept cool for the comfort of mothers and staff, but cool air can cause ELBW infants to lose heat through conduction and convection. Cold delivery rooms (less than 26C) have been associated with colder admission temperatures in the NICU for ELBW infants (Knobel, Wimmer, et al., 2005). Therefore, it is important that the NICU nurse attending an imminent delivery of an ELBW infant increases the thermostat setting to 80F (26C) upon arrival in the room, thus making the room warmer by the time the infant is delivered.

Caregiving During NICU Stabilization

In recent observations of 10 ELBW infants over their rst 12 hours in the NICU (Knobel, 2006), the observer sat by the infants bedside and recorded physiological data and information on the procedures experienced by the infant. Observer notes were compared to computer printouts of infant temperatures for the study period. A report of all physiological variables is in progress, but in the meantime, the clinical observations provide some valuable information. Temperatures during stabilization in the NICU were very low for most ELBW infants, and 7 of 10 infants averaged hypothermic (less than or equal to 36.4C) temperatures throughout the rst 12 hours after birth. Body temperatures as low as 33.0C were recorded. Infant temperatures dropped during caregiver procedures such as umbilical line insertions, intubations, obtaining chest x-rays, taking vital signs, manipulating intravenous lines, repositioning, and suctioning. Infant temperatures also were lower when humidity was not added to the incubator or when doors were open and humidity decreased. When the incubator or items placed next to the infant, such as blankets or snugglies, were not prewarmed, infant temperatures decreased. Temperatures also decreased when boluses of room temperature uids such as saline or blood were given. These clinical observations provide a reminder of how caregiving affects ELBW infants temperatures during the rst 12 hours in the NICU. Although NICU nurses have been taught about these issues in the past, it is easy to overlook environmental conditions during stabilization procedures in a critical situation. May/June 2007

the infant is transfused with new blood, dictate the use of blood warmed to 37C (Cloherty, Stark, & Eichenwald, 2003). If the ELBW infant needs a blood transfusion or saline bolus, the uid in a syringe can be warmed in the infants incubator prior to infusion.

ll NICU care providers should optimize the thermal environment for ELBW infants, especially during delivery room care and NICU stabilization.

In conclusion, it is important for all NICU care providers to optimize the thermal environment for ELBW infants, especially in the delivery room, during NICU stabilization, and through the rst 12 to 24 hours of life. These vulnerable patients are dependent on our actions to prevent cold stress and minimize heat loss during stabilization. Optimal thermal care may reduce morbidity and mortality for ELBW infants.

Acknowledgments
Supported by National Service Research Award, 1F31 NR09143-01, American Nurses Foundation, Nurses Charitable Trust District V FNA Scholar Research Grant, and Foundation of Neonatal Research and Education Research Grant. REFERENCES
American Academy of Pediatrics, & American Heart Association. (2005). Summary of major changes to the guidelines. 2005 AAP/AHA guidelines for neonatal resuscitation. Retrieved October 17, 2006, from http://www.aap.org/nrp/ nrpmain.html American Academy of Pediatrics, & College of Obstetrics and Gynecologists. (1988). Guidelines for perinatal care (2nd ed.). Elk Grove Village, IL: American Academy of Pediatrics. Anderson, P., Kleinman, C., Lister, G., & Talner, N. (1998). Cardiovascular function during normal fetal and neonatal development and with hypoxic stress. In R. Polin & W. Fox (Eds.), Fetal and neonatal physiology (2nd ed., vol. 1, pp. 837-889). Philadelphia: W.B. Saunders. Askin, D. (2002). Complications in the transition from fetal to neonatal life. Journal of Obstetric, Gynecologic, and Neonatal Nursing, 31, 318-327. Barrett, E. (2003). The thyroid gland. In W. Boron & E. Boulpaep (Eds.), Medical physiology: A cellular and molecular approach (pp. 1035-1048). Philadelphia: Saunders.

Cloherty, J., Stark, A., & Eichenwald, E. (Eds.). (2003). Manual of neonatal care (5th ed.). Philadelphia: LippincottWilliams & Wilkins. Cramer, K., Wiebe, N., Hartling, L., Crumley, E., & Vohra, S. (2005). Heat loss prevention: A systematic review of occlusive skin wrap for premature neonates. Journal of Perinatology, 25, 763-769. Day, R., Caliguiri, L., Kamenski, C., & Ehrlich, F. (1964). Body temperature and survival of premature infants. Pediatrics, 34, 171-181. Deshpande, S., & Platt, W. (1997). Association between blood lactate and acid-base status and mortality in ventilated babies. Archives of Diseases in Childhood, 76, F15-F20. Guyton, A., & Hall, J. (2006). Textbook of medical physiology (11th ed.). Philadelphia: W.B. Saunders. Hammarlund, K., & Sedin, G. (1979). Transepidermal water loss in newborn infants: III. Relation to gestation age. Acta Paediatrica Scandinavica, 68, 795-801. Hatai, S. (1902). On the presence in human embryos of an interscapular gland corresponding to the so-called hibernating gland of lower mammals. Anatomy Anzeiger, 21, 369. Hazan, J., Maag, U., & Chessex, P. (1991). Association between hypothermia and mortality rate of premature infants Revisited. American Journal of Obstetrics and Gynecology, 164, 111-112. Horns, K. (2002). Comparison of two microenvironments and nurse caregiving on thermal stability of ELBW infants. Advances in Neonatal Care, 2, 149-160. Houstek, J., Vizek, K., Pavelka, S., Kopecky, J., Krejcova, E., & Hermanska, J. (1993). Type II iodothyronine 5-deiodinase and uncoupling protein in brown adipose tissue of human newborns. Journal of Clinical Endocrinology Metabolism, 77, 382-387. Hull, D. (1977). Brown adipose tissue and the newborn infants response to cold. In E. Phill, J. Barnes, & M. Newton (Eds.), Scientic foundations of obstetrics and gynaecology (2nd ed, pp. 540-550). London: M. Heinemann Medical Books. Jones, E., & DeCherney, A. (2003). Fetal and neonatal physiology. In W. Boron & E. Boulpaep (Eds.), Medical physiology: A cellular and molecular approach (pp. 1190-1208). Philadelphia: Saunders. Knobel, R. (2006). Physiological effects of thermoregulation in ELBW infants (Doctoral dissertation, University of North Carolina at Chapel Hill, 2006). Dissertation Abstracts International, 1-223. (UMI Microform No. 3219434) Knobel, R., Vohra, S., & Lehmann, C. (2005). Heat loss prevention in the delivery room for preterm infants: A national survey of newborn intensive care units. Journal of Perinatology, 25, 514-518. Knobel, R., Wimmer, J., & Holbert, D. (2005). Heat loss prevention for preterm infants in the delivery room. Journal of Perinatology, 25, 304-309. Loughead, M., Loughead, J., & Reinhart, M. J. (1997). Incidence and physiologic characteristics of hypothermia in the very low birth weight infant. Pediatric Nursing, 23, 11-15. Lyon, A., Pikaar, M., Badger, P., & McIntosh, N. (1997). Temperature control in very low birthweight infants during rst ve days of life. Archives of Diseases in Childhood, 76, F47-F50.

286 JOGNN

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Malin, S., & Baumgart, S. (1987). Optimal thermal management for low birth weight infants nursed under high-powered radiant warmers. Pediatrics, 79, 47-54. Mathew, R. (1998). Development of the pulmonary circulation: Metabolic aspects. R. Polin & W. Fox (Eds.), Fetal and neonatal physiology (2nd ed., vol. 1, pp. 924-927). Philadelphia: W.B. Saunders Company. Mathews, T., & MacDorman, M. (2006). Infant mortality statistics from the 2003 period linked birth/infant death data set. National Vital Statistics Reports, 54, 1-30. Nadel, E.(2003). Regulation of body temperature. In W. Boron & E. Boulpaep (Eds.), Medical physiology (pp. 12311241). Philadelphia: Saunders. Nechad, M. (1986). Structure and development of brown adipose tissue. In P. Trayburn & D. Nicholls (Eds.), Brown adipose tissue (pp. 1-30). London, UK: Edward Arnold Publishers. Richardson, D., Corcoran, J., Escobar, G., & Lee, S. (2001). SNAP-II and SNAPPE-II: Simplied newborn illness severity and mortality risk scores. Journal of Pediatrics, 138, 92-100. Sauer, P. (1995). Metabolic background of neonatal heat production, energy balance, metabolic response to heat and cold. In A. Okken & J. Koch (Eds.), Thermoregulation of sick and low birth weight neonates (pp. 9-20). Berlin, Germany: Springer-Verlag. Sedin, G. (1995). Neonatal heat transfer, routes of heat loss and heat gain. In A. Okken & J. Koch (Eds.), Thermoregulation of sick and low birth weight neonates (pp. 21-36). Berlin, Germany: Springer-Verlag. Seri, I. (1998). Regulation of acid-base balance in the fetus and neonate. In R. Polin & W. Fox (Eds.), Fetal and neonatal physiology (2nd ed., vol. 2, pp. 1726-1730). Philadelphia: W.B. Saunders. Silverman, W., Fertig, J., & Berger, A. (1958). The inuence of the thermal environment upon the survival of newly born premature infants. Pediatrics, 22, 876-886.

Sinclair, J. C. (1992). Management of the thermal environment. In J. C. Sinclair & M. B. Bracken (Eds.), Effective care of the newborn infant (pp. 40-58). Oxford, UK: Oxford University Press. Thomas, K. (2003). Preterm infant thermal responses to caregiver differ by incubator control mode. Journal of Perinatology, 23, 640-645. Voet, D., Voet, J., & Pratt, C. (2002). Electron transport and oxidative phosphorylation. In D. Voet, J. Voet, & C. Pratt (Eds.), Fundamentals of biochemistry (Upgrade ed., pp. 492-528). New York: John Wiley & Sons. Vohra, S., Grent, G., Campbell, V., Abbott, M., & Whyte, R. (1999). Effect of polyethylene occlusive skin wrapping on heat loss in very low birth weight infants at delivery: A randomized trial. Journal of Pediatrics, 134, 547-551. Vohra, S., Roberts, R., Zhang, B., Janes, M., & Schmidt, B. (2004). Heat loss prevention (HeLP) in the delivery room: A randomized controlled trial of polyethylene occlusive skin wrapping in very preterm infants. Journal of Pediatrics, 145, 750-753. Widmaier, J., Raff, H., & Strang, K. (2005). Vanders human physiology: The mechanisms of body function (9th ed.). New York: McGraw-Hill Companies. Robin Knobel, PHD, RN, NNP, is a former assistant professor in the School of Nursing at the University of North Carolina, Chapel Hill, NC. Diane Holditch-Davis, PHD, RN, FAAN, is a professor in the School of Nursing at the Duke University, Durham, NC. Address for correspondence: Robin Knobel, PHD, RN, NNP, 408 Long Point Road, Chocowinity, NC 27817. E-mail: rbknobel@ earthlink.net.

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