DOI: 10.1542/peds.2006-0943 2007;119;e643-e649; originally published online Feb 12, 2007; Pediatrics

Network Abbot R. Laptook, Walid Salhab, Brinda Bhaskar and and the Neonatal Research

MorbiditiesAdmission Temperature of Low Birth Weight Infants: Predictors and Associated

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ARTICLE

Admission Temperature of Low Birth Weight Infants:Predictors and Associated MorbiditiesAbbot R. Laptook, MDa,b, Walid Salhab, MDc, Brinda Bhaskar, MSd, and the Neonatal Research Network

aDepartment of Pediatrics, Brown Medical School, Brown University, Providence, Rhode Island; bDepartment of Pediatrics, Women and Infants Hospital of Rhode Island,Providence, Rhode Island; cDepartment of Pediatrics, University of Texas Southwestern Medical Center, Dallas, Texas; dStatistics and Epidemiology Unit, Research TriangleInstitute, Research Triangle Park, North Carolina

The authors have indicated they have no financial relationships relevant to this article to disclose.

ABSTRACT

BACKGROUND. There is a paucity of information on the maintenance of body temper-ature at birth for low birth weight infants.

OBJECTIVES.We examined the distribution of temperatures in low birth weight in-fants on admission to the NICUs in the Neonatal Research Network centers anddetermined whether admission temperature was associated with antepartum andbirth variables and selected morbidities and mortality.

METHODS. Infants without major congenital anomalies born during 2002 and 2003with birth weights of 401 to 1499 g who were admitted directly from the deliveryroom to the NICU were included. Bivariate associations between antepartum/birthvariables and admission temperature and selected morbidities/mortality and ad-mission temperature were examined, followed by multivariable linear or logisticregressions to detect independent associations.

RESULTS. There were 5277 study infants and the mean (�SD) birth weight andgestational age were 1036 � 286 g and 28 � 3 weeks, respectively. The distributionof admission temperatures was 14.3% at �35°C, 32.6% between 35 and 35.9°C,42.3% between 36 and 36.9°C, and 10.8% at �37°C. The estimate of birth weighton admission temperature with and without intubation was �0.13°C and �0.04°Cper 100-g increase in birth weight, respectively. The mean admission temperaturefor each center varied from 1.5°C below to 0.3°C above a reference center. Onadjusted analyses, admission temperature was inversely related to mortality (28%increase per 1°C decrease) and late-onset sepsis (11% increase per 1°C decrease)but not to intraventricular hemorrhage, necrotizing enterocolitis, or duration ofconventional ventilation.

CONCLUSIONS. Preventing decreases in temperature at birth among low birth weightinfants remains a challenge. Associations with intubation and center of birthsuggest that assessment of temperature control for infants intubated in the deliveryroom may be beneficial. Whether the admission temperature is part of the casualpath or a marker of mortality needs additional study.

www.pediatrics.org/cgi/doi/10.1542/peds.2006-0943

doi:10.1542/peds.2006-0943

KeyWordstemperature, prematurity, low birthweight, sepsis

AbbreviationsNEC—necrotizing enterocolitisIVH—intraventricular hemorrhageOR—odds ratioCI—confidence interval

Accepted for publication Sep 20, 2006

Address correspondence to Abbot R. Laptook,MD, Women and Infants Hospital of RhodeIsland, Department of Pediatrics, 101 DudleySt, Suite 1100, Providence, RI 02905. E-mail:alaptook@wihri.org

PEDIATRICS (ISSN Numbers: Print, 0031-4005;Online, 1098-4275). Copyright © 2007 by theAmerican Academy of Pediatrics

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BIRTH IS ASSOCIATED with changes that affect thebody temperature of the newborn. These include

the ambient room temperature, multiple routes of heatloss (evaporative, convective, and conductive), and in-creases in oxygen consumption with consequent heatproduction.1–3 Heat loss usually far exceeds heat produc-tion after birth, and if measures are not initiated toreduce heat loss, body temperature will fall.4 An exces-sive fall in body temperature may impair the transitionfrom intrauterine to extrauterine circulatory pathwaysgiven the effect of temperature on pulmonary vasomo-tor tone and acid-base homeostasis.5,6 In general, effec-tive interventions to prevent cold stress for the terminfant are applied to the preterm infant, for example,drying and the use of radiant warmers4; however, ahigher surface area/weight ratio and skin characteristicsmake reducing heat loss for the preterm infant a moreformidable challenge.7 Current data on the relative suc-cess or failure in avoiding cold stress for preterm new-borns has been limited to the extremes of prematurity8

or small numbers of patients from third-world coun-tries.9 The purpose of this report was to use a largemulticenter cohort of low birth weight infants to deter-mine the following: (a) the frequency distribution oftemperatures on admission to NICUs, (b) the variables atbirth that are associated with the largest extent of re-duced admission temperature, and (c) whether admis-sion temperature is independently associated with se-lected neonatal morbidities and in-hospital mortality.

METHODSThe study was conducted among 15 centers of the Na-tional Institute of Child Health and Human Develop-ment Neonatal Research Network. Data were retrievedon all of the neonates with the following inclusion cri-teria: born at a network center between January 1, 2002,and December 31, 2003; born with a birth weight of 401to 1499 g; admitted directly to a NICU from a deliveryroom; and born without a major congenital anomaly.The first temperature obtained on admission of eachinfant to the NICU from the labor and delivery depart-ment was recorded as the admission temperature alongwith the date and time charted. Temperatures recordedin the delivery room or during transport to the NICUwere not recorded. The site of temperature measure-ment (axilla, skin, or rectal) was noted. Exclusion crite-ria were missing admission temperature, missing time ofadmission temperature, or temperature recorded after 2hours of age.

Data on each mother and infant were prospectivelycollected as part of an ongoing survey of neonatal mor-bidity and mortality initiated in 1987.10 Trained researchnurses reviewed the medical charts of mother and infantand entered predefined data items into an institutionalreview board-approved computerized database. Neona-tal outcome data were assessed at discharge from the

hospital, 120 days after birth, or at the time of death,using which ever came first.

Variables explored for associations with admissiontemperature included the following: (a) maternal vari-ables, including exposure to antibiotics (any use duringthe hospitalization for delivery), tocolytics, antenatalsteroids (partial or complete course), and the presence ofmultiple births; (b) intrapartum variables, including thepresence of labor, ruptured membranes �18 hours, andthe mode of delivery; (c) infant characteristics, includingbirth weight, gestational age (obstetric criteria), and gen-der; (d) delivery room variables, including intubationand/or chest compression with or without resuscitativemedications, Apgar scores, and umbilical artery pH andbase excess; (e) site (axilla, rectum, or skin) and age oftemperature measurements; and (f) network center ofbirth. Neonatal outcomes included days of conventionalventilation, late-onset sepsis (positive blood culture after72 hours of age), necrotizing enterocolitis (NEC; modi-fied Bell’s stage IIa or above),11 grade III or IV intraven-tricular hemorrhage (IVH), and death after 12 hours ofage and before hospital discharge. The assigned cause ofdeath reflects the purported underlying, proximate dis-ease process contributing to death and is based on au-topsy and clinical findings using predefined causes in themanual of operations for the database.

Data analysis for associations with admission temper-ature were initially explored with bivariate analyses be-tween admission temperature and maternal and intra-partum variables, infant characteristics, and deliveryroom events. Variables significant at a .10 level of sig-nificance in bivariate analyses were entered into multi-variable linear regressions. Umbilical artery pH and basedeficit were not included in the multivariable analysis,because values were available only for a subset of thecohort. Gestational age and chest compressions/resusci-tative medications were not included because of col-linearity with birth weight and intubation, respectively.One center was designated the reference center on thebasis of the highest percentage of admission tempera-tures between 36 and 36.9°C (center 10). Center resultsin multivariable analyses were expressed relative to cen-ter 10.

In a similar fashion, analyses for associations betweenadmission temperature and outcomes were initially ex-plored with bivariate analyses, and variables significantat a .10 level of significance were entered into multiva-riable linear regressions for continuous outcomes andlogistic regressions for categorical outcomes. These anal-yses were controlled for antenatal steroids, gender, race,birth weight, intubation, Apgar at 5 minutes, and center.Results of logistic regressions were expressed using oddsratios (ORs) and 95% confidence intervals (CIs). Resultsof multivariable linear regressions were expressed usingthe parameter estimate to indicate the magnitude ofindependent associations.

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RESULTSBetween January 1, 2002, and December 31, 2003,there were 7498 infants entered into the database. Ap-plying the inclusion criteria resulted in the exclusion of1649 infants, of which 1450 were excluded for 1 criteriaonly (749 outborn, 462 not directly admitted to anNICU, 207 with an anomaly, and 32 out of the weightrange). Applying the admission temperature criteria tothe remaining 5849 infants resulted in the exclusion of570 infants. Of the latter infants, 264 were consideredviable (given delivery room interventions, ventilatorsupport, intravenous fluids, etc), and 306 were nonvia-ble (no care provided). All but 59 of the 570 infantsexcluded for the temperature requirement had missingtemperature or time of temperature. Two additional in-fants fulfilled the temperature requirement but werenonviable and were excluded. The study cohort wascomposed of 5277 infants.

Descriptive characteristics of selected maternal andintrapartum variables, infant characteristics, and vari-ables from the delivery room are listed in Table 1. Infantsexcluded for not meeting the admission temperaturecriteria (n � 570) were of a lower birth weight (880 �318 and 545 � 151 g, mean � SD for viable and non-viable, respectively) and gestational age (26.3 � 3.2 and22.7 � 2.3 weeks for viable and nonviable, respectively).Umbilical artery blood gas results were available for 48%(pH data) and 46% (base deficit data) of the cohort. Themean admission temperature was 35.9 � 1.0°C (range:28–39.6°C). The distribution of admission temperaturesamong the cohort (Fig 1) demonstrates that 46.9% ofthe temperatures were �36°C. In contrast, the fre-quency of admission temperatures �37.0°C was 10.8%and �38°C was 1.3%. The frequency of admission tem-

peratures �35 and �36°C increased with decreasinggestational age and birth weight (Table 2). The measure-ment site of admission temperatures varied on the basisof center practice and was recorded from the axilla(77.6%), rectum (15.5%), and skin (7.0%); 9 patientshad missing data for this item. The mean age at theadmission temperature was 23 � 14 minutes with amedian value of 20 minutes (25th and 75th percentilesof 14 and 27 minutes, respectively).

Variables present before or at birth and associatedwith admission temperature on bivariate analyses weremultiple births, labor, use of antenatal steroids, maternalantibiotics, rupture of membranes, mode of delivery,birth weight, gestational age, center, intubation, 5-minute Apgar, site and age of temperature measure-ment, and center. Only the variables listed in Table 3were significantly associated with the admission temper-ature on multivariable analyses. Multiple births, use ofantenatal steroids, and prolonged rupture of membraneswere associated with a statistically significant but smallchange in admission temperature, each �0.2°C com-pared with the absence of the variable. A similar changein temperature was associated with age of temperaturemeasurement. In contrast, birth weight and intubation,center of birth, and the Apgar score at 5 minutes wereassociated with the largest change in admission temper-ature (Table 3). There was a significant interaction be-tween birth weight and intubation in the delivery room.The admission temperature was 0.04°C higher with each100-g increase in birth weight; however, for infantsrequiring intubation in the delivery room, the admissiontemperature was 0.13°C higher with each 100-g increasein birth weight. The admission temperature was 0.05°Chigher for each point increase in the Apgar score at 5minutes. The site of temperature measurement was as-sociated with the admission temperature in that rectaland axilla temperatures were 0.40 and 0.22°C higherthan skin temperature, respectively. Finally, there was aprominent association between center of birth and theadmission temperature. The average admission temper-ature of each of the 14 centers ranged from 0.3°C aboveto as much as 1.5°C below the average admission tem-perature of the reference center. The variability in thedistribution of admission temperatures among the 15centers is plotted in Fig 2.

The frequencies of selected neonatal morbidities forthis cohort were 6.3% for NEC, 10.3% for IVH grades IIIand IV, 23.3% for late-onset sepsis, and 10 � 18 days ofconventional ventilation. In-hospital mortality was12.2% with 45.2% of the deaths occurring at �7 days ofage. Major categories of assigned causes of death arelisted in Table 4. In multivariable analyses, there was noassociation between the admission temperature andNEC (OR: 1.0; CI: 0.90–1.16), grade III/IV IVH (OR:0.96; CI: 0.86–1.07), or duration of conventional venti-lation (0.4 days per 1°C decrease in the admission tem-

TABLE 1 Descriptive Characteristics of the Study Cohort

Characteristic Total

Maternal, %Medications receivedAntibiotics 69.9Tocolytics 42.1Antenatal steroids 82.6

Intrapartum, %Multiple births 28.0Labor 63.9Ruptured membranes �18 h 24.6Cesarean section 63.1

Infant characteristicsBirth weight, mean � SD, g 1032� 288Gestational age, mean � SD, wk 28.0� 2.8Male, % 51.2

Delivery roomApgar at 1 min �7, % 56.1Apgar at 5 min �7, % 24.9Umbilical artery pH, mean � SD 7.26� 0.11Umbilical artery base deficit, mean � SD �4.5� 4.3Intubation, % 52.4Chest compressions/medications, % 6.8

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perature; P � .1). In contrast, for every 1°C decrease inadmission temperature, the odds of late-onset sepsiswere increased by 11% (OR: 1.11; CI: 1.02–1.20), andthe odds of dying were increased by 28% (OR: 1.28; CI:1.16–1.41).

DISCUSSIONThis report documents the temperature on admission ofa recent large cohort of very low birth weight infantsborn within 15 academic centers and transferred directlyto the NICU from the labor and delivery department.The principal findings of this study are as follows: (a) lowtemperatures on admission are common; (b) there areimportant associations between the admission tempera-ture and variables antecedent to admission that may beamenable to change; and (c) there is a prominent asso-ciation between the extent of reduced temperature onadmission and both late-onset sepsis and in-hospitalmortality.

Efforts to limit heat loss are important initial steps inthe stabilization of newborns immediately after birthand are incorporated in the Neonatal Resuscitation Pro-gram12 and the World Health Organization’s guide tothermal control of the newborn.13 Minimizing heat lossin low birth weight and premature infants is difficultbecause of high evaporative heat loss exacerbated by alarge temperature gradient from the skin to the ambientair and physical characteristics of the premature infant(increased surface area/weight ratio, immature epider-mal barrier, limited vernix caseosa, and subcutaneousfat).14–18 There are relatively few reports on the fre-quency of low temperatures at birth among prematureinfants. Among hospitals in third-world nations, the fre-quency of temperatures �36°C at 2 hours after birth canbe as high as 60% for cohorts that include both term andlow birth weight infants, and these observations arelinked to a high incidence of hypothermia at 24 hours ofage.9,19,20 Even in developed countries, the frequency ofadmission temperature �35°C for all infants born before26 weeks’ gestation within the United Kingdom and theRepublic of Ireland during 1995 was 40% (EPICureStudy).8 The cohort of infants in the current report rep-resents a broader gestational age (21–42 weeks on the

FIGURE 1Results are presented for the distribution of admission tempera-tures among 5277 low birth weight infants irrespective of mea-surement site (axilla, rectum, or skin).

TABLE 2 Admission Temperature for Infants<28Weeks’ Gestation

GestationalAge, wk

n Birth Weight,mean � SD, g

AdmissionTemperature, %

�35°C �36°C

28 643 1088� 201 9.6 38.327 609 977� 182 10.7 41.526 539 840� 163 13.2 44.225 468 751� 130 20.5 57.124 397 655� 100 33.8 64.2

�24 187 598� 118 43.9 71.1

Data are presented up to 28 weeks, because the registry is defined by birth weight, and infants�28 weeks’ with a birth weight �1500 g will not be included.

TABLE 3 Multivariate Associations With Admission Temperature

Variable ParameterEstimate, °Ca

P

Multiple births 0.05 .045Use of antenatal steroids 0.10 .006Rupture of membranes �18 h 0.19 �.0001Mean age at admission temperature 0.17 .0023Intubation � birth weightb

Birth weight with intubation, per 100-g increase 0.13 �.0001Birth weight without intubation, per 100-g increase 0.04 �.0001

5-min Apgar score, per Apgar point increase 0.05 �.0001Center: lowest/highest average valuec �1.51/0.29 �.0001Measurement site: rectal/axillad 0.40/0.22 �.0001a The parameter estimate indicates the magnitude of change in temperature (oC) in the pres-ence of the variable listed. The overall model had an r2 value of 0.33 (P � .0001).b There was a significant interaction between birth weight and intubation that resulted indifferent parameter estimates for birth weight on the basis of the presence or absence ofintubation.c Values for each center are relative to the reference center. For simplicity, the centers with thelowest and highest average admission temperature are listed.d Values are relative to skin temperature.

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basis of obstetric criteria; mean of 28 weeks) defined bybirth weight (�1499 g) and may account for the lowerfrequency of admission temperatures �35°C (14.3%).However, in this cohort, �47% of the admission tem-peratures were �36°C. An important limitation of thisstudy is the observational design without a standardpractice regarding site, time, device, and technique usedfor temperature measurements. In addition, no data areavailable on the maternal temperature at the time of orimmediately proximate to delivery, the temperature ofthe delivery room, or the qualifications of the pediatricproviders in attendance.

Interventions to minimize the extent of heat loss havebeen studied in small groups of infants. The most effec-tive seems to be occlusive wraps for which there hasbeen interest over the past 30 years.21 More recently, 3randomized clinical trials demonstrated that the use of

polyethylene wraps or polyurethane bags comparedwith drying in the delivery room prevented heat loss andbetter maintained rectal admission temperatures for in-fants �29 weeks’ gestation.22–24 Additional measures in-clude the use of caps, which have been demonstrated toreduce the exchange of heat between the head and theambient air.25,26 The use of caps conveniently comple-ments the application of occlusive wraps where heat lossfrom the exposed head is still a concern. Important ques-tions regarding the use of occlusive wraps are whetherthere are low-frequency adverse effects on the skin,alterations in skin flora, or potential overheating of thebody. Systematic reviews and formal meta-analysis sug-gest that elevated temperatures recorded on NICU ad-mission among wrapped infants may reflect factors suchas maternal temperature and infection rather than oc-clusive wraps and indicate the need for additional stud-ies.27,28 Information regarding the use of occlusive wrapsor other means to reduce heat loss from the currentcohort was not collected as part of this study. Given thefrequency of low admission temperatures among infantsin this report, surveillance of temperatures in the deliv-ery room and on admission would seem to be an appro-priate, worthwhile, quality improvement initiative.

Variables antecedent to and independently associatedwith prominent changes in admission temperature werebirth weight and intubation, Apgar score at 5 minutes,and center of birth. The association with birth weightwas expected, because the physical characteristics of lowbirth weight infants predispose to a mismatch betweenheat production and heat exchange with the ambientenvironment when high-risk infants are stabilized atbirth.14 This is consistent with the EPICure Study, where

FIGURE 2Admission temperatures (axilla, rectum, or skin) of eachcenter are plotted as the percentage of measurements inthe following temperature strata: black, �35°C; gray, 35to 35.9°C; white, 36 to 36.9°C; and striated white, �37°C.Center 10 is the reference center on the basis of the high-est percentage of temperatures between 36 and 36.9°C(74%).

TABLE 4 Causes of Death

Causea n

Respiratory distressIsolated 88With severe intracranial hemorrhage 71With infection 49

NEC 47with sepsis 42

Sepsis (early and late onset) 70Bronchopulmonary dysplasiaIsolated 26With infection 29With brain injury 10

Severe intracranial hemorrhage 16Immaturity 46a These causes represent 77% of the 642 deaths in this cohort of 5277 infants. The remainder ofthe assigned causes reflects multiple conditions or suspected diagnoses.

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an admission temperature �35°C occurred in 30%,43%, and 58% of infants of 25, 24, and 23 weeks’gestation (median birth weights of 760, 680, and 600 g,respectively).8 Multivariate analysis in the present studyindicates that the effect of birth weight alone is relativelysmall, with an average of a 0.4°C difference in admissiontemperature between infants with birth weights of 401and 1499 g. In contrast, if intubation is performed, theeffect of birth weight is an average of 1.4°C differentbetween infants of the same 2 birth weights. The asso-ciation of the Apgar score at 5 minutes may parallel thebirth weight-intubation interaction, because lower Ap-gar scores may represent a proxy for infants having moreresuscitative measures (of which the most common pro-cedure is intubation) or the response to such interven-tions. Center of birth was associated with a prominentchange in admission temperature relative to the refer-ence center. Five of the 14 centers had an average ad-mission temperature �0.75°C lower than the referencecenter, and 3 centers were �1°C lower. Delineation ofthe specific practices for maintenance of temperature inthe delivery room at each center was not part of thisstudy, but the results suggest that a quality improvementapproach using benchmark initiatives may be helpful forsome centers.

The admission temperature was not associated withNEC, severe IVH, or duration of conventional venti-lation. Associations were present between admissiontemperature and both late-onset sepsis and in-hospitalmortality. Thermal management has been labeled a cor-nerstone of neonatology.29 The latter is based on thepioneering work of Silverman et al30 that maintenance ofbody temperature through control of the thermal envi-ronment during the first 5 days of life (isolette temper-ature of 29 vs 32°C with resultant axillary temperaturesof 31.1 vs 33.7°C, respectively) reduced mortality in lowbirth weight infants. Other clinical trials of low birthweight infants yielded similar observations.31–33 Thesetherapeutic trials outlined the effects of a thermal man-agement scheme on mortality rather than an associationbetween admission temperature and outcome.

Additional temperatures beyond admission to theNICU were not collected on infants in the present co-hort. Whether prevention of low temperatures at birthdecreases mortality or whether the low admission tem-perature is part of the casual path or simply a marker foran increase in the odds of mortality cannot be deter-mined from this observational analysis. Previous inves-tigations that have reported associations between admis-sion temperature and mortality have insufficient samplesize,22 were not adjusted for covariates,34 and were notreproducible.23 The association in this report betweenadmission temperature and late-onset sepsis provides apotential path to link the admission temperature andmortality. In adults, a self-limited interval of periopera-tive hypothermia may promote postoperative infections

via temperature-mediated impaired immune function35;perioperative normothermia decreased the postopera-tive infectious complication.36 Whether late-onset sepsisremote from birth is causally linked to admission tem-perature is unknown. In addition, the causes of death(Table 4) seem to reflect expected complications of pre-maturity.

The results of this observational cohort demonstratethat minimizing the extent of temperature reduction atbirth for the low birth weight and premature infantremains challenging. The birth weight-intubation inter-action with the admission temperature and the variabil-ity among the various participating centers suggest thatthermal control for newborns requiring respiratory sup-port at birth requires a reassessment of practice. Thetime, effort, and resources to determine whether avoid-ance of temperature reductions at birth reduces mortal-ity seem to be well justified in view of a potential casualpath via late-onset sepsis.

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