Admission Temperature of Low Birth Weight Infants: Predictors and Associated

Morbidities
Abbot R. Laptook, Walid Salhab, Brinda Bhaskar and and the Neonatal Research
Network
Pediatrics 2007;119;e643-e649; originally published online Feb 12, 2007;
DOI: 10.1542/peds.2006-0943

The online version of this article, along with updated information and services, is
located on the World Wide Web at:
http://www.pediatrics.org/cgi/content/full/119/3/e643

PEDIATRICS is the official journal of the American Academy of Pediatrics. A monthly

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ARTICLE

Admission Temperature of Low Birth Weight Infants:

Predictors and Associated Morbidities
Abbot 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 Triangle
Institute, Research Triangle Park, North Carolina

The authors have indicated they have no nancial 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-

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

fants on admission to the NICUs in the Neonatal Research Network centers and
determined whether admission temperature was associated with antepartum and
birth variables and selected morbidities and mortality.

doi:10.1542/peds.2006-0943

METHODS. Infants without major congenital anomalies born during 2002 and 2003

Abbreviations
NECnecrotizing enterocolitis
IVHintraventricular hemorrhage
OR odds ratio
CI condence interval

with birth weights of 401 to 1499 g who were admitted directly from the delivery
room to the NICU were included. Bivariate associations between antepartum/birth
variables and admission temperature and selected morbidities/mortality and admission temperature were examined, followed by multivariable linear or logistic
regressions to detect independent associations.
RESULTS. There were 5277 study infants and the mean (SD) birth weight and

gestational age were 1036 286 g and 28 3 weeks, respectively. The distribution
of admission temperatures was 14.3% at 35C, 32.6% between 35 and 35.9C,
42.3% between 36 and 36.9C, and 10.8% at 37C. The estimate of birth weight
on admission temperature with and without intubation was 0.13C and 0.04C
per 100-g increase in birth weight, respectively. The mean admission temperature
for each center varied from 1.5C below to 0.3C above a reference center. On
adjusted analyses, admission temperature was inversely related to mortality (28%
increase per 1C decrease) and late-onset sepsis (11% increase per 1C decrease)
but not to intraventricular hemorrhage, necrotizing enterocolitis, or duration of
conventional ventilation.

Key Words
temperature, prematurity, low birth
weight, sepsis

Accepted for publication Sep 20, 2006

Address correspondence to Abbot R. Laptook,
MD, Women and Infants Hospital of Rhode
Island, Department of Pediatrics, 101 Dudley
St, Suite 1100, Providence, RI 02905. E-mail:
alaptook@wihri.org
PEDIATRICS (ISSN Numbers: Print, 0031-4005;
Online, 1098-4275). Copyright 2007 by the
American Academy of Pediatrics

CONCLUSIONS. Preventing decreases in temperature at birth among low birth weight

infants remains a challenge. Associations with intubation and center of birth

suggest that assessment of temperature control for infants intubated in the delivery
room may be beneficial. Whether the admission temperature is part of the casual
path or a marker of mortality needs additional study.
PEDIATRICS Volume 119, Number 3, March 2007

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e643

IRTH IS ASSOCIATED with changes that affect the

body temperature of the newborn. These include

the ambient room temperature, multiple routes of heat
loss (evaporative, convective, and conductive), and increases in oxygen consumption with consequent heat
production.13 Heat loss usually far exceeds heat production after birth, and if measures are not initiated to
reduce heat loss, body temperature will fall.4 An excessive fall in body temperature may impair the transition
from intrauterine to extrauterine circulatory pathways
given the effect of temperature on pulmonary vasomotor tone and acid-base homeostasis.5,6 In general, effective interventions to prevent cold stress for the term
infant are applied to the preterm infant, for example,
drying and the use of radiant warmers4; however, a
higher surface area/weight ratio and skin characteristics
make reducing heat loss for the preterm infant a more
formidable challenge.7 Current data on the relative success or failure in avoiding cold stress for preterm newborns has been limited to the extremes of prematurity8
or small numbers of patients from third-world countries.9 The purpose of this report was to use a large
multicenter cohort of low birth weight infants to determine the following: (a) the frequency distribution of
temperatures on admission to NICUs, (b) the variables at
birth that are associated with the largest extent of reduced admission temperature, and (c) whether admission temperature is independently associated with selected neonatal morbidities and in-hospital mortality.
METHODS
The study was conducted among 15 centers of the National Institute of Child Health and Human Development Neonatal Research Network. Data were retrieved
on all of the neonates with the following inclusion criteria: born at a network center between January 1, 2002,
and December 31, 2003; born with a birth weight of 401
to 1499 g; admitted directly to a NICU from a delivery
room; and born without a major congenital anomaly.
The first temperature obtained on admission of each
infant to the NICU from the labor and delivery department was recorded as the admission temperature along
with the date and time charted. Temperatures recorded
in the delivery room or during transport to the NICU
were not recorded. The site of temperature measurement (axilla, skin, or rectal) was noted. Exclusion criteria were missing admission temperature, missing time of
admission temperature, or temperature recorded after 2
hours of age.
Data on each mother and infant were prospectively
collected as part of an ongoing survey of neonatal morbidity and mortality initiated in 1987.10 Trained research
nurses reviewed the medical charts of mother and infant
and entered predefined data items into an institutional
review board-approved computerized database. Neonatal outcome data were assessed at discharge from the
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LAPTOOK et al

hospital, 120 days after birth, or at the time of death,

using which ever came first.
Variables explored for associations with admission
temperature included the following: (a) maternal variables, including exposure to antibiotics (any use during
the hospitalization for delivery), tocolytics, antenatal
steroids (partial or complete course), and the presence of
multiple births; (b) intrapartum variables, including the
presence of labor, ruptured membranes 18 hours, and
the mode of delivery; (c) infant characteristics, including
birth weight, gestational age (obstetric criteria), and gender; (d) delivery room variables, including intubation
and/or chest compression with or without resuscitative
medications, Apgar scores, and umbilical artery pH and
base excess; (e) site (axilla, rectum, or skin) and age of
temperature measurements; and (f) network center of
birth. Neonatal outcomes included days of conventional
ventilation, late-onset sepsis (positive blood culture after
72 hours of age), necrotizing enterocolitis (NEC; modified Bells stage IIa or above),11 grade III or IV intraventricular hemorrhage (IVH), and death after 12 hours of
age and before hospital discharge. The assigned cause of
death reflects the purported underlying, proximate disease process contributing to death and is based on autopsy and clinical findings using predefined causes in the
manual of operations for the database.
Data analysis for associations with admission temperature were initially explored with bivariate analyses between admission temperature and maternal and intrapartum variables, infant characteristics, and delivery
room events. Variables significant at a .10 level of significance in bivariate analyses were entered into multivariable linear regressions. Umbilical artery pH and base
deficit were not included in the multivariable analysis,
because values were available only for a subset of the
cohort. Gestational age and chest compressions/resuscitative medications were not included because of collinearity with birth weight and intubation, respectively.
One center was designated the reference center on the
basis of the highest percentage of admission temperatures between 36 and 36.9C (center 10). Center results
in multivariable analyses were expressed relative to center 10.
In a similar fashion, analyses for associations between
admission temperature and outcomes were initially explored with bivariate analyses, and variables significant
at a .10 level of significance were entered into multivariable linear regressions for continuous outcomes and
logistic regressions for categorical outcomes. These analyses were controlled for antenatal steroids, gender, race,
birth weight, intubation, Apgar at 5 minutes, and center.
Results of logistic regressions were expressed using odds
ratios (ORs) and 95% confidence intervals (CIs). Results
of multivariable linear regressions were expressed using
the parameter estimate to indicate the magnitude of
independent associations.

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RESULTS
Between January 1, 2002, and December 31, 2003,
there were 7498 infants entered into the database. Applying the inclusion criteria resulted in the exclusion of
1649 infants, of which 1450 were excluded for 1 criteria
only (749 outborn, 462 not directly admitted to an
NICU, 207 with an anomaly, and 32 out of the weight
range). Applying the admission temperature criteria to
the remaining 5849 infants resulted in the exclusion of
570 infants. Of the latter infants, 264 were considered
viable (given delivery room interventions, ventilator
support, intravenous fluids, etc), and 306 were nonviable (no care provided). All but 59 of the 570 infants
excluded for the temperature requirement had missing
temperature or time of temperature. Two additional infants fulfilled the temperature requirement but were
nonviable and were excluded. The study cohort was
composed of 5277 infants.
Descriptive characteristics of selected maternal and
intrapartum variables, infant characteristics, and variables from the delivery room are listed in Table 1. Infants
excluded for not meeting the admission temperature
criteria (n 570) were of a lower birth weight (880
318 and 545 151 g, mean SD for viable and nonviable, respectively) and gestational age (26.3 3.2 and
22.7 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. The
mean admission temperature was 35.9 1.0C (range:
28 39.6C). The distribution of admission temperatures
among the cohort (Fig 1) demonstrates that 46.9% of
the temperatures were 36C. In contrast, the frequency of admission temperatures 37.0C was 10.8%
and 38C was 1.3%. The frequency of admission tem-

TABLE 1 Descriptive Characteristics of the Study Cohort

Characteristic
Maternal, %
Medications received
Antibiotics
Tocolytics
Antenatal steroids
Intrapartum, %
Multiple births
Labor
Ruptured membranes 18 h
Cesarean section
Infant characteristics
Birth weight, mean SD, g
Gestational age, mean SD, wk
Male, %
Delivery room
Apgar at 1 min 7, %
Apgar at 5 min 7, %
Umbilical artery pH, mean SD
Umbilical artery base decit, mean SD
Intubation, %
Chest compressions/medications, %

Total

69.9
42.1
82.6
28.0
63.9
24.6
63.1
1032 288
28.0 2.8
51.2
56.1
24.9
7.26 0.11
4.5 4.3
52.4
6.8

peratures 35 and 36C increased with decreasing

gestational age and birth weight (Table 2). The measurement site of admission temperatures varied on the basis
of center practice and was recorded from the axilla
(77.6%), rectum (15.5%), and skin (7.0%); 9 patients
had missing data for this item. The mean age at the
admission temperature was 23 14 minutes with a
median value of 20 minutes (25th and 75th percentiles
of 14 and 27 minutes, respectively).
Variables present before or at birth and associated
with admission temperature on bivariate analyses were
multiple births, labor, use of antenatal steroids, maternal
antibiotics, rupture of membranes, mode of delivery,
birth weight, gestational age, center, intubation, 5minute Apgar, site and age of temperature measurement, and center. Only the variables listed in Table 3
were significantly associated with the admission temperature on multivariable analyses. Multiple births, use of
antenatal steroids, and prolonged rupture of membranes
were associated with a statistically significant but small
change in admission temperature, each 0.2C compared with the absence of the variable. A similar change
in temperature was associated with age of temperature
measurement. In contrast, birth weight and intubation,
center of birth, and the Apgar score at 5 minutes were
associated with the largest change in admission temperature (Table 3). There was a significant interaction between birth weight and intubation in the delivery room.
The admission temperature was 0.04C higher with each
100-g increase in birth weight; however, for infants
requiring intubation in the delivery room, the admission
temperature was 0.13C higher with each 100-g increase
in birth weight. The admission temperature was 0.05C
higher for each point increase in the Apgar score at 5
minutes. The site of temperature measurement was associated with the admission temperature in that rectal
and axilla temperatures were 0.40 and 0.22C higher
than skin temperature, respectively. Finally, there was a
prominent association between center of birth and the
admission temperature. The average admission temperature of each of the 14 centers ranged from 0.3C above
to as much as 1.5C below the average admission temperature of the reference center. The variability in the
distribution of admission temperatures among the 15
centers is plotted in Fig 2.
The frequencies of selected neonatal morbidities for
this cohort were 6.3% for NEC, 10.3% for IVH grades III
and IV, 23.3% for late-onset sepsis, and 10 18 days of
conventional ventilation. In-hospital mortality was
12.2% with 45.2% of the deaths occurring at 7 days of
age. Major categories of assigned causes of death are
listed in Table 4. In multivariable analyses, there was no
association between the admission temperature and
NEC (OR: 1.0; CI: 0.90 1.16), grade III/IV IVH (OR:
0.96; CI: 0.86 1.07), or duration of conventional ventilation (0.4 days per 1C decrease in the admission temPEDIATRICS Volume 119, Number 3, March 2007

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e645

FIGURE 1
Results are presented for the distribution of admission temperatures among 5277 low birth weight infants irrespective of measurement site (axilla, rectum, or skin).

TABLE 2 Admission Temperature for Infants <28 Weeks Gestation

Gestational
Age, wk

Birth Weight,
mean SD, g

28
27
26
25
24
24

643
609
539
468
397
187

1088 201
977 182
840 163
751 130
655 100
598 118

Admission
Temperature, %
35C

36C

9.6
10.7
13.2
20.5
33.8
43.9

38.3
41.5
44.2
57.1
64.2
71.1

Data are presented up to 28 weeks, because the registry is dened 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
Multiple births
Use of antenatal steroids
Rupture of membranes 18 h
Mean age at admission temperature
Intubation birth weightb
Birth weight with intubation, per 100-g increase
Birth weight without intubation, per 100-g increase
5-min Apgar score, per Apgar point increase
Center: lowest/highest average valuec
Measurement site: rectal/axillad

Parameter
Estimate, Ca
0.05
0.10
0.19
0.17
0.13
0.04
0.05
1.51/0.29
0.40/0.22

P
.045
.006
.0001
.0023
.0001
.0001
.0001
.0001
.0001

a The parameter estimate indicates the magnitude of change in temperature (oC) in the presence of the variable listed. The overall model had an r2 value of 0.33 (P .0001).
b There was a signicant interaction between birth weight and intubation that resulted in
different parameter estimates for birth weight on the basis of the presence or absence of
intubation.
c Values for each center are relative to the reference center. For simplicity, the centers with the
lowest and highest average admission temperature are listed.
d Values are relative to skin temperature.

perature; P .1). In contrast, for every 1C decrease in

admission temperature, the odds of late-onset sepsis
were increased by 11% (OR: 1.11; CI: 1.021.20), and
the odds of dying were increased by 28% (OR: 1.28; CI:
1.16 1.41).
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LAPTOOK et al

DISCUSSION
This report documents the temperature on admission of
a recent large cohort of very low birth weight infants
born within 15 academic centers and transferred directly
to the NICU from the labor and delivery department.
The principal findings of this study are as follows: (a) low
temperatures on admission are common; (b) there are
important associations between the admission temperature and variables antecedent to admission that may be
amenable to change; and (c) there is a prominent association between the extent of reduced temperature on
admission and both late-onset sepsis and in-hospital
mortality.
Efforts to limit heat loss are important initial steps in
the stabilization of newborns immediately after birth
and are incorporated in the Neonatal Resuscitation Program12 and the World Health Organizations guide to
thermal control of the newborn.13 Minimizing heat loss
in low birth weight and premature infants is difficult
because of high evaporative heat loss exacerbated by a
large temperature gradient from the skin to the ambient
air and physical characteristics of the premature infant
(increased surface area/weight ratio, immature epidermal barrier, limited vernix caseosa, and subcutaneous
fat).1418 There are relatively few reports on the frequency of low temperatures at birth among premature
infants. Among hospitals in third-world nations, the frequency of temperatures 36C at 2 hours after birth can
be as high as 60% for cohorts that include both term and
low birth weight infants, and these observations are
linked to a high incidence of hypothermia at 24 hours of
age.9,19,20 Even in developed countries, the frequency of
admission temperature 35C for all infants born before
26 weeks gestation within the United Kingdom and the
Republic of Ireland during 1995 was 40% (EPICure
Study).8 The cohort of infants in the current report represents a broader gestational age (21 42 weeks on the

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

TABLE 4 Causes of Death

a

Cause

Respiratory distress
Isolated
With severe intracranial hemorrhage
With infection
NEC
with sepsis
Sepsis (early and late onset)
Bronchopulmonary dysplasia
Isolated
With infection
With brain injury
Severe intracranial hemorrhage
Immaturity

88
71
49
47
42
70
26
29
10
16
46

a These causes represent 77% of the 642 deaths in this cohort of 5277 infants. The remainder of
the assigned causes reects multiple conditions or suspected diagnoses.

basis of obstetric criteria; mean of 28 weeks) defined by

birth weight (1499 g) and may account for the lower
frequency of admission temperatures 35C (14.3%).
However, in this cohort, 47% of the admission temperatures were 36C. An important limitation of this
study is the observational design without a standard
practice regarding site, time, device, and technique used
for temperature measurements. In addition, no data are
available on the maternal temperature at the time of or
immediately proximate to delivery, the temperature of
the delivery room, or the qualifications of the pediatric
providers in attendance.
Interventions to minimize the extent of heat loss have
been studied in small groups of infants. The most effective seems to be occlusive wraps for which there has
been interest over the past 30 years.21 More recently, 3
randomized clinical trials demonstrated that the use of

polyethylene wraps or polyurethane bags compared

with drying in the delivery room prevented heat loss and
better maintained rectal admission temperatures for infants 29 weeks gestation.2224 Additional measures include the use of caps, which have been demonstrated to
reduce the exchange of heat between the head and the
ambient air.25,26 The use of caps conveniently complements the application of occlusive wraps where heat loss
from the exposed head is still a concern. Important questions regarding the use of occlusive wraps are whether
there are low-frequency adverse effects on the skin,
alterations in skin flora, or potential overheating of the
body. Systematic reviews and formal meta-analysis suggest that elevated temperatures recorded on NICU admission among wrapped infants may reflect factors such
as maternal temperature and infection rather than occlusive wraps and indicate the need for additional studies.27,28 Information regarding the use of occlusive wraps
or other means to reduce heat loss from the current
cohort was not collected as part of this study. Given the
frequency of low admission temperatures among infants
in this report, surveillance of temperatures in the delivery room and on admission would seem to be an appropriate, worthwhile, quality improvement initiative.
Variables antecedent to and independently associated
with prominent changes in admission temperature were
birth weight and intubation, Apgar score at 5 minutes,
and center of birth. The association with birth weight
was expected, because the physical characteristics of low
birth weight infants predispose to a mismatch between
heat production and heat exchange with the ambient
environment when high-risk infants are stabilized at
birth.14 This is consistent with the EPICure Study, where
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e647

an admission temperature 35C 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 study
indicates that the effect of birth weight alone is relatively
small, with an average of a 0.4C difference in admission
temperature between infants with birth weights of 401
and 1499 g. In contrast, if intubation is performed, the
effect of birth weight is an average of 1.4C different
between infants of the same 2 birth weights. The association of the Apgar score at 5 minutes may parallel the
birth weight-intubation interaction, because lower Apgar scores may represent a proxy for infants having more
resuscitative measures (of which the most common procedure is intubation) or the response to such interventions. Center of birth was associated with a prominent
change in admission temperature relative to the reference center. Five of the 14 centers had an average admission temperature 0.75C lower than the reference
center, and 3 centers were 1C lower. Delineation of
the specific practices for maintenance of temperature in
the delivery room at each center was not part of this
study, but the results suggest that a quality improvement
approach using benchmark initiatives may be helpful for
some centers.
The admission temperature was not associated with
NEC, severe IVH, or duration of conventional ventilation. Associations were present between admission
temperature and both late-onset sepsis and in-hospital
mortality. Thermal management has been labeled a cornerstone of neonatology.29 The latter is based on the
pioneering work of Silverman et al30 that maintenance of
body temperature through control of the thermal environment during the first 5 days of life (isolette temperature of 29 vs 32C with resultant axillary temperatures
of 31.1 vs 33.7C, respectively) reduced mortality in low
birth weight infants. Other clinical trials of low birth
weight infants yielded similar observations.3133 These
therapeutic trials outlined the effects of a thermal management scheme on mortality rather than an association
between admission temperature and outcome.
Additional temperatures beyond admission to the
NICU were not collected on infants in the present cohort. Whether prevention of low temperatures at birth
decreases mortality or whether the low admission temperature is part of the casual path or simply a marker for
an increase in the odds of mortality cannot be determined from this observational analysis. Previous investigations that have reported associations between admission temperature and mortality have insufficient sample
size,22 were not adjusted for covariates,34 and were not
reproducible.23 The association in this report between
admission temperature and late-onset sepsis provides a
potential path to link the admission temperature and
mortality. In adults, a self-limited interval of perioperative hypothermia may promote postoperative infections
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LAPTOOK et al

via temperature-mediated impaired immune function35;

perioperative normothermia decreased the postoperative infectious complication.36 Whether late-onset sepsis
remote from birth is causally linked to admission temperature is unknown. In addition, the causes of death
(Table 4) seem to reflect expected complications of prematurity.
The results of this observational cohort demonstrate
that minimizing the extent of temperature reduction at
birth for the low birth weight and premature infant
remains challenging. The birth weight-intubation interaction with the admission temperature and the variability among the various participating centers suggest that
thermal control for newborns requiring respiratory support at birth requires a reassessment of practice. The
time, effort, and resources to determine whether avoidance of temperature reductions at birth reduces mortality seem to be well justified in view of a potential casual
path via late-onset sepsis.
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e649

Admission Temperature of Low Birth Weight Infants: Predictors and Associated

Morbidities
Abbot R. Laptook, Walid Salhab, Brinda Bhaskar and and the Neonatal Research
Network
Pediatrics 2007;119;e643-e649; originally published online Feb 12, 2007;
DOI: 10.1542/peds.2006-0943
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