Hypothermia and Early Neonatal Mortality in Preterm Infants

Maria Fernanda Branco de Almeida, MD, PhD1, Ruth Guinsburg, MD, PhD1, Guilherme Assis Sancho, MD1,
Izilda Rodrigues Machado Rosa, MD, PhD2, Zeni Carvalho Lamy, MD, PhD3, Francisco Eul
ogio Martinez, MD, PhD4,
Regina Paula Guimar~aes Vieira Cavalcante da Silva, MD, PhD5, L
gia Silvana Lopes Ferrari, MD, PhD6,
Ligia Maria Suppo de Souza Rugolo, MD, PhD7, V^ania Olivetti Steffen Abdallah, MD, PhD8, and
Rita de C
assia Silveira, MD, PhD9, on behalf of Brazilian Network on Neonatal Research*
Objective To evaluate intervention practices associated with hypothermia at both 5 minutes after birth and at
neonatal intensive care unit (NICU) admission and to determine whether hypothermia at NICU admission is associated with early neonatal death in preterm infants.
Study design This prospective cohort included 1764 inborn neonates of 22-33 weeks without malformations
admitted to 9 university NICUs from August 2010 through April 2012. All centers followed neonatal International
Liaison Committee on Resuscitation recommendations for the stabilization and resuscitation in the delivery room
(DR). Variables associated with hypothermia (axillary temperature <36.0 C) 5 minutes after birth and at NICU admission, as well as those associated with early death, were analyzed by logistic regression.
Results Hypothermia 5 minutes after birth and at NICU admission was noted in 44% and 51%, respectively, with
6% of early neonatal deaths. Adjusted for confounding variables, practices associated with hypothermia at 5 minutes after birth were DR temperature <25 C (OR 2.13, 95% CI 1.67-2.28), maternal temperature at delivery
<36.0 C (OR 1.93, 95% CI 1.49-2.51), and use of plastic bag/wrap (OR 0.53, 95% CI 0.40-0.70). The variables associated with hypothermia at NICU admission were DR temperature <25 C (OR 1.44, 95% CI 1.10-1.88), respiratory
support with cold air in the DR (OR 1.40, 95% CI 1.03-1.88) and during transport to NICU (OR 1.51, 95% CI 1.082.13), and cap use (OR 0.55, 95% CI 0.39-0.78). Hypothermia at NICU admission increased the chance of early
neonatal death by 1.64-fold (95% CI 1.03-2.61).
Conclusion Simple interventions, such as maintaining DR temperature >25 C, reducing maternal hypothermia
prior to delivery, providing plastic bags/wraps and caps for the newly born infants, and using warm resuscitation
gases, may decrease hypothermia at NICU admission and improve early neonatal survival. (J Pediatr
2014;164:271-5).

reterm infants are susceptible to hypothermia shortly after birth. Laptook et al1 found that 47% of 5277 very low birth
weight (VLBW) infants had a body temperature <36 C on admission to the neonatal intensive care unit (NICU).
Adjusted analyses showed that admission temperature was inversely related to intrahospital mortality, with a 28% increase in mortality per 1 C decrease in body temperature. Moderate and severe hypothermia were associated with the risk of
death before hospital discharge in a population-based cohort of 8782 VLBW infants in California NICUs in 2006 and 2007.2
Neither study reported the practices applied to maintain normal body temperature from birth to NICU admission. According to McCall et al,3 plastic wraps or
bags and plastic caps are effective in reducing heat losses in infants born at <28From the Division of Neonatal Medicine, Universidade
~o Paulo/Escola Paulista de Medicina, Sa
~o
Federal de Sa
29 weeks gestation, but it is unclear whether they reduce the risk of death.
Paulo; Department of Pediatrics, Universidade Estadual


de Campinas/Hospital da Mulher Prof. Dr. Jose
The Neonatal Task Force of the International Liaison Committee on ResusciAristodemo Pinotti, Campinas, SP, Brazil; Department
~o/
of Public Health, Universidade Federal do Maranha
tation recommended in 2010 Consensus on Science that newborn infants of <28

rio, Sa
~o Lu
s, MA, Brazil; Department
Hospital Universita
weeks gestation should be completely covered in a polythene wrap or bag up to
~o Paulo/Hospital das
of Pediatrics, Universidade de Sa
~o Preto, Ribeira
~o Preto, SP, Brazil;
Cl
nicas de Ribeira
their necks without drying immediately after birth and then placed under a
Department of Pediatrics, Universidade Federal do

/Hospital de Cl
nicas, Curitiba; Department of
Parana
radiant heater and resuscitated or stabilized in a standard fashion. Infants should
Pediatrics and Pediatric Surgery, Universidade Estadual
be kept wrapped until admission and temperature check. Hyperthermia should

rio, Londrina, PR, Brazil;
de Londrina/Hospital Universita
Department of Pediatrics, Faculdade de Medicina de
be avoided. Delivery room (DR) temperatures should be at least 26 C for infants
Botucatu da Universidade Estadual Paulista, Botucatu,
SP, Brazil; Department of Pediatrics, Universidade
of <28 weeks gestation.4 However, all of these recommendations have low levels
^ndia/Hospital de Cl
nicas, Uberla
^ndia,
Federal de Uberla
MG, Brazil; and Department of Pediatrics, Universidade
of evidence regarding their efficacy and effectiveness in reducing neonatal morFederal do Rio Grande do Sul/Hospital de Cl
nicas de
tality.
Porto Alegre, Porto Alegre, RS, Brazil
1

*List of members of the Brazilian Network on Neonatal

Research is available at www.jpeds.com (Appendix).

DR
NICU
VLBW

Delivery room
Neonatal intensive care unit
Very low birth weight

Supported by Conselho Nacional de Desenvolvimento

gico (472827-2009-0). The authors
Cient
fico e Tecnolo
declare no conflicts of interest.
0022-3476/$ - see front matter. Copyright 2014 Mosby Inc.
All rights reserved. http://dx.doi.org/10.1016/j.jpeds.2013.09.049

271

THE JOURNAL OF PEDIATRICS

www.jpeds.com

Our goal is to evaluate intervention practices associated

with hypothermia at 5 minutes after birth and at NICU
admission and to determine whether hypothermia at NICU
admission is associated with early neonatal death in preterm
infants.

Methods
We conducted a multicenter prospective cohort study of infants born at gestational ages of 230/7 to 336/7 weeks without
congenital anomalies and admitted at 9 centers of the Brazilian Network on Neonatal Research between August 2010 and
April 2012. All of the centers are level III public university
hospitals and serve as referral centers for high-risk pregnancies. All of the hospitals have NICU beds and the staff, equipment, and infrastructure required to treat critically ill
neonates. The study was approved by the institutional review
boards of each institution, and informed consent was signed
by the mother of each enrolled neonate.
At each NICU, 1 neonatologist prospectively collected
maternal and neonatal data in a Web-based data system
specially designed for the study. Gestational age was defined
by the hierarchy of obstetric measures (last menstrual period,
followed by first trimester ultrasonography) and a neonatal
exam.5 The centers followed the Neonatal Resuscitation
Program of the Brazilian Pediatric Society guidelines for stabilization and resuscitation at birth according to the International Liaison Committee on Resuscitation Consensus on
Science and Treatment Recommendations.4,6 All of the centers
used the same types of digital environmental (Term^
ometro
Digital 7665; Incoterm, Porto Alegre, Brazil) and individual
thermometers (Medflex; Incoterm, Porto Alegre, Brazil). DR
temperature was registered at birth. Axillary maternal temperature was assessed up to 20 minutes before delivery; axillary
neonatal temperature was measured 5 minutes after birth
and at NICU admission. Both maternal and neonatal hypothermia were defined as a body temperature <36.0 C. The
neonatal thermal care practices analyzed were the following:
use of a plastic bag or wrap; use of a linen or woolen cap;
use of heated gases for ventilation; and use of a transport incubator. Care of all newly born infants was given under radiant
heaters in the DR, and exothermic mattresses were not used.
The main outcomes were hypothermia 5 minutes after
birth, hypothermia at NICU admission, and death by 6
days after birth. Stepwise logistic regression was applied to
evaluate the variables associated with these outcomes. For hypothermia 5 minutes after birth, maternal and neonatal characteristics at birth and variables related to neonatal thermal
care in the DR were considered to be independent variables.
For hypothermia at NICU admission, variables related to
thermal care during transport from the DR to the NICU
were also included. For early neonatal death, maternal and
neonatal characteristics at birth, hypothermia at NICU
admission, and neonatal morbidity were evaluated as independent variables. Variables with a value of P < .20 in the univariate analysis were included in the initial model. The fitness
272

Vol. 164, No. 2

of the model was assessed by use of the Hosmer-Lemeshow
test. We calculated that a study population of 1660 patients
would be required to detect a difference of 3% in early
neonatal mortality (exposed, 8%; nonexposed, 5%) considering a b error of 20%, an a error of 5%, and a ratio of
exposed/nonexposed to hypothermia at NICU admission
of 1:1.

Results
During the study period, 1955 inborn preterm infants with
gestational ages of 23-33 weeks and without congenital
anomalies satisfied our inclusion criteria, and 1764 (90%)
were enrolled in the study. Enrollment varied from 115 to
262 neonates per center. Axillary temperature at 5 minutes
after birth was measured in 1374 neonates, and hypothermia
was noted in 44% (median 36.0 C; 25th-75th percentiles
35.5 C-36.4 C). Axillary temperature at NICU admission
was measured in 1764 neonates at an average of 32 minutes
after birth, and hypothermia was noted in 51% (median
35.9 C; 25th-75th percentiles 35.3 C-36.4 C).
Hypothermia 5 minutes after birth and at NICU admission
varied among centers from 13% to 62% (P < .001) and from
25% to 75% (P < .001), respectively (Figure). Hypothermia
at 5 minutes after birth and at NICU admission was inversely
related to gestational age (P < .001), but 35% of neonates
with gestational ages of 32 and 33 weeks were hypothermic at
5 minutes, and z40% were hypothermic at NICU admission.
Early neonatal death occurred in 6% of the 1764 neonates,
varying among centers between 4% and 9% (P = .478).
Maternal and neonatal characteristics, including thermal
neonatal care practices, in infants with and without
hypothermia at 5 minutes after birth and at NICU
admission are shown in Table I. Median DR temperature
was 24.8 C (25th-75th percentiles 23.7 C-25.8 C); median
maternal axillary temperature was 36.2 C (25th-75th
percentiles 35.8 C-36.6 C; 9 mothers had temperature
$38 C) at an average of 18 minutes prior birth; and
median transport incubator temperature was 36.1 C (25th75th percentiles 35.0 C-37.0 C). Among the 1764 neonates,
9 (0.5%) had hyperthermia ($38.0 C) at NICU admission.
DR temperature <25 C, administration of cold air during
positive pressure ventilation, and endotracheal intubation
soon after birth were associated with hypothermia at 5
minutes of life and at NICU admission (Table I). The
following practices were also associated with hypothermia
at NICU admission: absence of cap, transport from DR to
NICU with cold air, and temperature of the transport
incubator <35 C.
Demographic and clinical characteristics of the patients,
according to early neonatal mortality, are shown in
Table II. Male sex, gestational age <28 weeks, birth weight
<1000 g, 1-minute Apgar score <4, 5-minute Apgar score
<7, hypothermia at NICU admission, Neonatal Acute
Physiology, Perinatal Extension, Version II score >40,
respiratory distress syndrome, air leaks, and grades III/IV
de Almeida et al

ORIGINAL ARTICLES

February 2014

Figure. Frequency of hypothermia at 5 minutes after birth, hypothermia at NICU admission, and early neonatal death per study
center and per gestational age (number of patients given in parentheses).

intraventricular hemorrhage were more frequent in newborn

infants who died in the first week after birth.
The independent variables associated with the main outcomes are shown in Table III. The final logistic models
were adjusted for birth center. The HosmerLemeshow
goodness-of-fit test values for hypothermia at 5 minutes
after birth, hypothermia at NICU admission, and early
neonatal death were 0.959, 0.939, and 0.495, respectively.
Adjusted for confounders, the DR temperature <25 C,
maternal hypothermia, and absence of plastic bag/wrap
were independent risk factors for hypothermia 5 minutes
after birth. In turn, hypothermia 5 minutes after birth was
strongly associated with hypothermia at NICU admission.
Absence of cap use and administration of cold air during
resuscitation and transport were also independent risk
factors for hypothermia at NICU admission. Hypothermia
at NICU admission increased the chance of early neonatal
death by 64%.

Discussion
In this cohort of inborn preterm infants born at 23-33 weeks
of gestational age, the incidence of hypothermia 5 minutes after birth was extremely high and was independently associated with low DR temperature, maternal hypertension,
maternal hypothermia, lower gestational age, and lack of
plastic bag/wrap. The presence of hypothermia soon after
birth was the main contributor to hypothermia at NICU
admission, which increased the chance of early neonatal
death by 64%. These results add to the current evidence in
the literature arguing for the urgency of initiating practices
to maintain normothermia as soon as the preterm neonate
is born. These practices include the following: maintenance
of DR temperature >25 C, careful assessment of maternal
temperature, use of a radiant heater in the DR, use of plastic
bag/wrap and cap, respiratory support with humidified and

Table I. Maternal and neonatal characteristics in infants with and without hypothermia 5 minutes after birth and at
NICU admission
Hypothermia at 5 min

Maternal age <20 y

Prenatal care $6 visits
Maternal hypertension
Antenatal steroids
Multiple gestation
Spinal anesthesia
Maternal hypothermia
Cesarean delivery
DR <25 C
Male sex
Gestational age <32 wk
Birth weight <1500 g
Use of plastic bag/wrap
Use of cap
PPV with cold air at DR
Endotracheal intubation
Hypothermia at 5 min
Transport incubator <35 C
Transport on O2/CPAP/MV
NICU admission >30 min

Present
(n = 606)

Absent
(n = 768)

21%
42%
42%
74%
21%
71%
39%
72%
63%
50%
68%
71%
61%
77%
58%
36%
-

19%
50%
30%
68%
23%
70%
24%
69%
47%
54%
53%
50%
59%
79%
48%
20%
-

Hypothermia at admission
P value

Present
(n = 894)

Absent
(n = 870)

P value

.253
.003
<.001
<.001
.170
.447
<.001
.110
.001
.120
<.001
<.001
.228
.190
<.001
<.001
-

20%
40%
40%
71%
20%
67%
33%
70%
60%
52%
68%
70%
54%
65%
57%
34%
70%
25%
81%
43%

19%
49%
27%
66%
25%
70%
28%
68%
47%
53%
53%
50%
55%
77%
46%
20%
22%
20%
68%
44%

.579
<.001
<.001
.004
.006
.190
.054
.627
<.001
.719
<.001
<.001
.564
<.001
<.001
<.001
<.001
.025
<.001
.687

O2/CPAP/MV, free-flow oxygen or continuous positive airway pressure or mechanical ventilation; PPV, positive pressure ventilation.

Hypothermia and Early Neonatal Mortality in Preterm Infants

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Table II. Maternal and neonatal characteristics of

preterm infants according to early neonatal mortality
Early neonatal death

Maternal age <20 y

Prenatal care $6 visits
Maternal hypertension
Peripartum infection
Multiple gestation
Antenatal steroids
Cesarean delivery
Male sex
Gestational age <28 wk
Birth weight <1000 g
Small for gestational age
1-min Apgar score 0-3
5-min Apgar score 0-6
Hypothermia at NICU admission
SNAPPE II >40
Respiratory distress syndrome
Air leaks
Persistent ductus arteriosus
Intraventricular hemorrhage III/IV
Culture-proved sepsis
Necrotizing enterocolitis

Table III. Logistic regression analysis for independent

variables associated with the main study outcomes
Outcome

Present
(n = 109)

Absent
(n = 1655)

P value

19%
30%
38%
23%
15%
59%
62%
64%
69%
78%
35%
53%
36%
72%
64%
88%
18%
28%
21%
10%
2%

20%
46%
34%
19%
23%
69%
69%
52%
15%
20%
28%
19%
11%
49%
10%
57%
4%
26%
4%
9%
2%

.900
.002
.398
.301
.046
.026
.127
.010
<.001
<.001
.141
<.001
<.001
<.001
<.001
<.001
<.001
.649
<.001
.735
.699

SNAPPE II, Score for Neonatal Acute Physiology, Perinatal Extension, Version II.

heated gases from birth until NICU admission, and use of

transport incubator with adequate temperature control. It
should be noted that these practices must be considered for
preterm infants with gestational age of 29-33 weeks, because
this study shows a high frequency of hypothermia 5 minutes
after birth and at NICU admission in this group of patients.
Environmental cold temperature has been associated with
higher odds of hypothermia at NICU admission in preterm
infants; however, the ideal DR temperature is unknown. Knobel et al7 performed a post-hoc analysis of preterm infants
with gestational age <29 weeks under radiant heaters randomized to receive or not receive polyurethane bags and showed
that room temperatures $26 C were associated with higher
admission temperatures in both the intervention and control
groups. According to Jia et al,8 an increase in the room temperature to an average of 25.1 C from a control room temperature of 22.5 C was associated with a 0.5 C higher mean
NICU admission rectal temperature and a decrease in the
incidence of hypothermia in preterm infants with gestational
age #32 weeks who were warmed under radiant heaters. The
present study provides further evidence to support the maintenance of DR temperatures at $25 C because the odds of hypothermia at 5 minutes after birth and at NICU admission
were 2.13 and 1.44 times greater, respectively, when the
room temperature was below this threshold.
A newly born infants body temperature is associated with
maternal temperature9; in fact, maternal fever and/or hyperthermia has been associated with high neonatal body temperatures.10 It is intuitive to assume that maternal hypothermia
would conversely be associated with neonatal hypothermia
soon after birth, but this association has not been demonstrated consistently. We show that maternal hypothermia
274

Vol. 164, No. 2

Hypothermia 5 min after birth

DR temperature <25 C
Gestational age <32 wk
Maternal hypertension
Maternal temperature at delivery <36 C
Use of plastic bag/wrap
Hypothermia at NICU admission
Hypothermia 5 min after birth
Maternal hypertension
Transport on O2/CPAP/MV
DR temperature <25 C
PPV with cold air in the DR
Use of cap
Early neonatal death
Gestational age <28 wk
Respiratory distress syndrome
5-min Apgar score 0-6
Male sex
Hypothermia at NICU admission
Antenatal steroids

OR (95% CI)
2.13 (1.67-2.28)
2.01 (1.51-2.68)
2.00 (1.55-2.59)
1.93 (1.49-2.51)
0.53 (0.40-0.70)
7.45 (5.70-9.73)
1.77 (1.34-2.33)
1.51 (1.08-2.13)
1.44 (1.10-1.88)
1.40 (1.03-1.88)
0.55 (0.39-0.78)
7.77 (4.87-12.41)
2.40 (1.28-4.51)
1.87 (1.17-3.00)
1.84 (1.19-2.85)
1.64 (1.03-2.61)
0.59 (0.38-0.91)

prior to delivery nearly doubles the chance that a newly born

infant will present a body temperature <36 C at 5 minutes after birth, indicating that maternal thermal care is an important
measure for the prevention of neonatal hypothermia.
In the present study, the use of a plastic bag/wrap independently decreased the chance of hypothermia at 5 minutes after
birth by 47%, and the use of cotton cap decreased the chance
of hypothermia at NICU admission by 45%. A Cochrane Review article3 indicates that the use of plastic bag or wrap soon
after birth in preterm infants with gestational age <28 weeks
decreases the likelihood of body temperature <36.0 C at
NICU admission by 34% (OR 0.66, 95% CI 0.51%-0.84%).
In the literature, the efficacy of cap use to decrease hypothermia in newly born preterm infants is controversial.3 A randomized clinical trial of 96 preterm infants born at a
gestational age <29 weeks showed similar axillary temperature at NICU admission when patients under a radiant heater
received only a polyethylene cap (36.1 C  1.4 C) or only a
polyethylene occlusive skin wrapping (35.8 C  1.6 C).11
A study by the Eunice Kennedy Shriver National Institute of
Child Health and Human Development Neonatal Network
that included 9565 preterm infants born between 22 and 28
weeks gestation showed that 67% required ventilation by
endotracheal tube at birth.12 Among preterm neonates who
do not need resuscitation, respiratory stabilization with
noninvasive continuous positive airway pressure is increasingly applied in the DR.13 However, the warming and humidification of inspired gases for invasive and noninvasive
ventilation in neonates are not routine for neonatal resuscitation.14 In the present study, all of the patients who received
any respiratory support in the DR and during transport to the
NICU received cold humidified air. The use of positive pressure ventilation with cold air in the DR and at transport
increased the chance of hypothermia at NICU admission
by 1.40-fold (95% CI 1.03-fold to 1.88-fold) and 1.51-fold
(95% CI 1.08-fold to 2.13-fold), respectively. Te Pas et al15
de Almeida et al

February 2014
analyzed 2 cohorts of preterm infants born at #32 weeks of
gestational age. In the first period, respiratory support from
birth to NICU admission was performed with cold air, and
the mean rectal temperature at admission was 35.9 C 
0.6 C. In the second period, heated and humidified gas was
introduced for respiratory support, and admission temperature increased to 36.4 C  0.6 C. These findings suggest that
the delivery of heated humidified gases in the DR and during
neonatal transport may play an important role in decreasing
the frequency of hypothermia after birth.
The studies that provide evidence of the association between hypothermia at NICU admission and neonatal mortality are either retrospective or secondary analyses of data
collected to evaluate other primary outcomes. In a Malaysian
VLBW study group with 868 patients, the chance of hospital
mortality was 1.26 times (95% CI 1.06-1.50 times) greater for
infants with body temperature <36.5 C at NICU admission.16
The Epicure study, which included 811 neonates born at <25
weeks, showed that body temperature <35 C at NICU admission increased the chance of hospital death by 1.72-fold (95%
CI 1.17-fold to 2.56-fold).17 The chance of death rose 1.28fold (95% CI 1.16-fold to 1.41-fold) for each 1 C decrease
in temperature at NICU admission in 5277 VLBW infants
admitted to Eunice Kennedy Shriver National Institute of
Child Health and Human Development Neonatal Network
Centers.1 Miller et al studied 8782 VLBW infants and found
a 1.5-fold (95% CI 1.3-fold to 1.9-fold) increase in the chance
of hospital death for neonates admitted to the NICU with
body temperature <36 C.2 Our study, which was prospectively designed to verify an association between early neonatal
mortality and hypothermia at NICU admission, showed that
the chance of early neonatal death is 1.64-fold (1.03-2.61)
higher in infants with admission temperatures <36 C,
adjusted for birth center and for other maternal and neonatal
variables that contribute to early mortality, such as gestational
age, sex, perinatal asphyxia, respiratory distress syndrome,
and the absence of antenatal steroid treatment. However, as
noted by Laptook and Watkinson,18 it remains unclear
whether hypothermia at NICU admission is a cause of
neonatal mortality or a marker of high patient acuity.
As this was an observational cohort study, the results
shown here reflect only associations. However, as a careful
prospective observation of practices applied to thermal care
in the daily routine of the studied DRs, it provides a picture
of the magnitude of the problem and the independent protective practices that may decrease hypothermia at 5 minutes
after birth and at NICU admission. Simple interventions,
such as maintaining a DR temperature >25 C, reducing
maternal hypothermia prior to delivery, using plastic bags/
wraps and caps for the newly born infants, and using warm
resuscitation gases, may decrease hypothermia at NICU
admission and improve early neonatal survival. n

ORIGINAL ARTICLES
coordinator; Instituto Fernandes Figueira of Fundacao Osvaldo Cruz,
Rio de Janeiro, Brazil), for helping with the logistic management of the
Brazilian Network on Neonatal Research.
Submitted for publication Jun 17, 2013; last revision received Aug 22, 2013;
accepted Sep 20, 2013.
Reprint requests: Ruth Guinsburg, MD, PhD, Rua Vicente Felix 77, apt 09, CEP
~o Paulo, SP, Brazil. E-mail: ruthgbr@netpoint.com.br
01410-020, Sa

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and Cynthia Magluta, MD (Brazilian Network on Neonatal Research

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www.jpeds.com

Vol. 164, No. 2

Appendix
Additional members of the Brazilian Network on Neonatal
Research include:
Universidade Estadual de Campinas/Hospital da Mulher
Prof. Dr. Jos
e Aristodemo Pinotti: S
ergio Tadeu Martins
Marba, MD, PhD, Ana Cristina Pinto, MD, Andrea Eliana
Lovato Cassone, MD, Jamil Pedro de Siqueira Caldas, MD,
PhD; Universidade Federal do Maranh~ao/Hospital Universit
ario: Maryn
ea do Vale Nunes, MD, Ana Claudia Garcia
Marques, MD; Universidade de S~ao Paulo/Hospital das
Cl
nicas de Ribeir~ao Preto: Ana Beatriz Goncalves, MD, Walusa Assad Goncalves Ferri, MD, PhD; Universidade Federal
do Paran
a/Hospital de Cl
nicas: Paulyne Stadler Venzon,
MD; Universidade Estadual de Londrina/Hospital Universit
ario: Angela Sara Jamusse de Brito, MD, Ana Berenice Ribeiro Carvalho, MD, Maria Rafaela Conde Gonzalez, MD;
Faculdade de Medicina de Botucatu da Universidade Estadual Paulista: Maria Regina Bentlin, MD, PhD, Glauce Regina
Fernandes Giacoia, MD; Universidade Federal de Uberl^andia/Hospital de Cl
nicas: Daniela Marques de Lima Mota
Ferreira, MD, Helo
sio dos Reis, MD; Universidade Federal
do Rio Grande do Sul/Hospital de Cl
nicas de Porto Alegre:
Renato S Procianoy, MD, PhD.

275.e1

de Almeida et al