hypothermia in very low birth weight infants

ORIGINAL ARTICLE

Hypothermia in very low birth weight infants: distribution,risk factors and outcomesSS Miller1, HC Lee2 and JB Gould1

1Department of Pediatrics, Division of Neonatal and Developmental Medicine, Stanford University, Palo Alto, CA, USA and2Department of Pediatrics, Division of Neonatology, University of California, San Francisco, CA, USA

Objective: The objective of this study was to study the epidemiology of

neonatal hypothermia in preterm infants using World Health Organization

(WHO) temperature criteria.

Study Design: A population-based cohort of 8782 very low birth weight

(VLBW) infants born in California neonatal intensive care units in 2006

and 2007. Associations between admission hypothermia and maternal and

neonatal characteristics and outcomes were determined using logistic

regression.

Result: In all, 56.2% of infants were hypothermic. Low birth weight,

cesarean delivery and a low Apgar score were associated with

hypothermia. Spontaneous labor, prolonged rupture of membranes and

antenatal steroid administration were associated with decreased risk of

hypothermia. Moderate hypothermia was associated with higher risk of

intraventricular hemorrhage (IVH). Moderate and severe hypothermic

conditions were associated with risk of death.

Conclusion: Hypothermia by WHO criteria is prevalent in VLBW infants

and is associated with IVH and mortality. Use of WHO criteria could guide

the need for quality improvement projects targeted toward the most

vulnerable infants.

Journal of Perinatology (2011) 31, S49–S56; doi:10.1038/jp.2010.177

Keywords: prematurity; neonatal intensive care units; risk assessment

Introduction

In both developed and developing countries, hypothermia is animportant risk factor for morbidity and mortality in newborns.1–5

The World Health Organization (WHO) established criteria forassessing hypothermia and published a guidebook on the thermalprotection of newborns in 1997, indicating that this issue is aworldwide problem even for term infants, particularly in developingnations.6 WHO classifications of hypothermia are (1) cold stress ormild hypothermia: 36.0 to 36.4 1C (96.8 to 97.51 F); (2) moderate

hypothermia: 32.0 to 35.9 1C (89.6 to 96.61 F); and (3) severehypothermia: below 32 1C (<89.61 F). The purpose of this studywas to assess the validity of the WHO classifications in the contextof a contemporary neonatal intensive care setting. Specifically, wewanted to (1) determine the distribution of neonatal hypothermiaas defined by WHO in a population-based cohort of VLBW infants;(2) identify the clinical associations and risk factors for theseclassifications; and (3) assess the degree to which neonatalmorbidities and mortalities were independently associated with theWHO hypothermia classifications. A better understanding of the riskfactors for and the mortality and morbidities associated with coldstress, moderate and severe hypothermia in this fragile populationis critical to designing appropriate advocacy and neonatal practiceinterventions to promote normothermia.

Patients and methods

The California Perinatal Quality Care Collaborative (CPQCC)collects clinical data in a prospective manner for infants born in127 member hospitals. Membership is offered to any hospital inCalifornia that provides neonatal intensive care. In the study periodfrom 1 January 2006 to 31 December 2007, greater than 90% ofCalifornia’s very low birth weight (VLBW) infants were cared for inCPQCC hospitals, creating a unique data set. This study wasapproved by the Stanford University Institutional Review Board.

The CPQCC conducts yearly data abstractor trainings atlocations throughout California. Each record has a variety of rangeand logic checks both at the time of data collection and before datacloseout, and records with excessive missing data are audited.

During the study period, there were 11 664 VLBW infants bornwith birth weight less than 1500 g. Of them, infants with agestational age (GA) less than 23 weeks (n¼ 492) or unknownGA (n¼ 13) or born with a birth weight less than 400 g (n¼ 37)were excluded. Patients born at non-CPQCC hospitals andsubsequently transferred to a CPQCC member hospital wereexcluded (n¼ 1522). Infants with neurological or gastrointestinalcongenital anomalies such as anencephaly, meningomyelocele,encephalocele, gastroschisis or omphalocele (n¼ 34) were

Correspondence: Dr SS Miller, Department of Pediatrics, Division of Neonatal and

Developmental Medicine, Stanford University, 750 Welch Road, Suite 315, Palo Alto,

CA 94304, USA.

E-mail: [email protected]

Journal of Perinatology (2011) 31, S49–S56

r 2011 Nature America, Inc. All rights reserved. 0743-8346/11

www.nature.com/jp

http://dx.doi.org/10.1038/jp.2010.177

mailto:[email protected]

http://www.nature.com/jp

excluded because of the risk for increased evaporative losses. Alsoexcluded were infants who had no temperature recorded in the firsthour (n¼ 482) or who died in the delivery room and had notemperature recorded (n¼ 302). There were 8782 infants in thefinal analytical cohort.

The first temperature on admission was standardized by theCPQCC guidelines. The infant’s core body temperature wasmeasured and recorded within the first hour after admission tothe neonatal intensive care unit. The temperature in degreesCentigrade to the nearest tenth of a degree was recorded. If theinfant’s temperature was measured several times within the firsthour after admission, the first temperature measurement value wasentered into the database. For centers that measure temperature indegrees Fahrenheit, a Fahrenheit-to-Centigrade conversion tablewas provided. Rectal temperature was the preferred value; however,if unavailable, esophageal, tympanic or axillary temperature wasrecorded.

The admission temperature and outcomes described below wererecorded at the hospital of birth. If an infant was subsequentlytransferred within the first 28 days after birth, the outcomes thatoccurred at the transfer hospital were recorded and included in ouranalyses. If an infant was transported after 28 days, the majority ofwhom would have been transported for convalescent care, anyoutcomes that occurred during the period at this second hospitalwere not recorded, with the exception of the outcome of death,which was reported regardless of transport status. If an infanttransported after 28 days developed morbidity that was seriousenough to warrant readmission, these outcomes were recorded andincluded in the analysis.

A cross-sectional data analysis was conducted to examine thedistribution, predictors and outcomes associated with neonatalhypothermia. Temperature criteria were based on the WHOclassifications of hypothermia and are defined as follows: (1) coldstress or mild hypothermia, 36.0 to 36.4 1C (96.8 to 97.51 F);(2) moderate hypothermia, 32.0 to 35.9 1C (89.6 to 96.61 F); and(3) severe hypothermia, below 32 1C (<89.61 F). TemperaturesX38.0 1C were considered as fever. Because of the low number ofinfants with temperature <32 1C (n¼ 9), severe and moderatehypothermia were combined into one category. Predictor variableswere as follows: maternal and intrapartum variables (age, race/ethnicity, prenatal care, antenatal steroids, spontaneous labor,multiple births, delivery mode, maternal or uterine infection,prolonged rupture of membranes (PROM) and hypertension);infant characteristics (gender, birth weight, gestational age) anddelivery room variables (Apgar scores, resuscitation includingoxygen administration, CPAP, bag-mask ventilation, chestcompressions and epinephrine administration). Low Apgar scoreswere defined as an assigned value <7. Neonatal outcome measuresincluded necrotizing enterocolitis, severe retinopathy of prematurity(ROP stage 3 or 4), oxygen dependence at 36-week-correctedgestational age, early (on or before day 3) and late (after day 3)

culture-positive bacterial sepsis, severe intraventricular hemorrhage(IVH grade 3 or 4 determined by any modality used to image thebrain on or before day 28 of life) and ultimate disposition(discharge home or death). Necrotizing enterocolitis was defined asone or more clinical signs (bilious gastric aspirate or emesis,abdominal distention or occult or gross blood in stool withno apparent rectal fissure) and one or more radiographicfindings (pneumatosis intestinalis, hepatobiliary gas orpneumoperitoneum). ROP stage 3 was defined as the presence of aridge with extraretinal fibrovascular proliferation and stage 4 wasdefined as partial retinal detachment. Grade 3 IVH was defined asintraventricular blood with ventricular dilation and Grade 4 wasdefined as intraparenchymal hemorrhage.

Associations between predictor variables and hypothermiawere tested in a bivariate analysis, followed by stepwise logisticregression. Separate models were constructed for combined severeand moderate, mild and severe hypothermia. We then studied thepotential contribution of hypothermia to neonatal outcomes.Separate models were constructed for neonatal outcomes in whichsevere, moderate or mild hypothermia was the independentvariable. Relevant factors were entered into forward stepwisemultivariable logistic regression models with an entry criteriaa-level of 0.05 to give odds ratios and 95% confidence limits forthose variables associated with hypothermia. Statistical analyseswere computed using SAS 9.1 (SAS, Cary, NC, USA).

Results

The cohort of 8782 infants had a mean (±s.d.) birth weight andGA of 1072±278 g and 28.4±2.8 weeks, respectively. The meanadmission temperature was 36.3 1C (s.d. 0.8), with a range of 26.1to 39.6 1C; 30.5% were mildly hypothermic, 25.6% were moderatelyhypothermic, 0.1% were severely hypothermic, 43.0% werenormothermic and 0.8% were noted to have a temperatureX38.0 1C (Figure 1).

The incidence of hypothermia was greatest and the meanadmission temperature lowest with decreasing GA and birth weight. Inall, 78.7% of infants born at 23 weeks and 82.8% of infants with abirth weight of 400 to 499 g were hypothermic. As GA and birth weightincreased, there was a decrease in the percentage of moderatehypothermia and an increase in the percentage of cold stress. Themean admission temperature also increased with birth weight andgestational age, with stabilization occurring after 26 weeks andbetween 800 and 899 g gestation (Appendix Tables A1 and A2).

Descriptive characteristics for the total study cohort, withdivision into normothermic, mild and moderate/severehypothermic infants, are listed in Table 1.

Risk factors for hypothermiaOn bivariate analysis, black (P¼ 0.0001) Hispanic (P¼ 0.0025)and other/unknown (P¼ 0.04) races were associated with

Hypothermia in very low birth weight infantsSS Miller et al

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Journal of Perinatology

hypothermia, as were maternal hypertension, Cesarean section andlow 1- and 5-min Apgar scores (P<0.0001). Antenatal steroid use(P<0.001), PROM (P<0.001), spontaneous labor (P<0.001),multiple births (P¼ 0.006) and uterine infection (P<0.001) wereassociated with normothermia. There were no associationsfound with Asian race, maternal age, gender, prenatal care ormaternal infection. Similar risk factors were seen for cold stress(details on request).

Using forward stepwise logistic regression, models were createdfor the combined category of moderate/severe hypothermia,for cold stress and for any hypothermia as compared withnormothermia (Table 2). For the outcome of moderate/severehypothermia, the most notable effect came from birth weight, withincreasing odds of hypothermia associated with decreasing birthweight between 400 and 999 g. Cesarean mode of delivery,low 1- and 5-min Apgar scores, maternal hypertension and Blackrace carried higher odds of moderate/severe hypothermia.Spontaneous labor, PROM and antenatal steroid administrationwere associated with lower odds of moderate-to-severe hypothermia,independent of birth weight.

Factors associated with the development of cold stress weresimilar to those of moderate/severe hypothermia. The model forsevere/moderate hypothermia showed decreasing odds withincreasing birth weight, whereas the cold stress model hadstatistically stable odds across birth weight categories.

Neonatal outcomesWe evaluated the relationship between hypothermia and stage 3or 4 ROP, necrotizing enterocolitis, early-onset sepsis, late-onset

sepsis, oxygen use at 36-week-corrected gestational age, IVH, deathand the combined outcome of grades 3 to 4 IVH and death.Table 3 shows the frequency of these morbidities across WHOtemperature criteria. Although there were significant bivariateassociations between hypothermia and ROP, late-onset sepsis,oxygen at 36 weeks, IVH and death, many of these relationshipswere not statistically significant after risk adjustment. After riskadjustment, we found no association between mild hypothermiaand any of the morbidities or death. Moderate hypothermia wasassociated with higher odds of IVH (odds ratio 1.3, 95% confidencelimit 1.1 to 1.6) and death (odds ratio 1.5, 95% confidence limit1.3 to 1.9). Severe hypothermia, although seen in only nineinfants, was also associated with higher odds of death (odds ratio5.6, 95% confidence limit 1.1 to 28.1).

Discussion

This study evaluated transitional hypothermia in a population-based cohort of VLBW infants born in California neonatal intensivecare units using the WHO classifications of hypothermia: cold stressor mild hypothermia, 36.0 to 36.4 1C (96.8 to 97.5 1F); moderatehypothermia, 32.0 to 35.9 1C (89.6 to 96.6 1F); and severehypothermia, below 32 1C (<89.6 1F). We found that cold stressand moderate hypothermia on admission were very common (30.5and 25.6%, respectively), whereas severe hypothermia was seenin only 0.1% of VLBWs. Both cold stress and moderate/severehypothermia were associated with various maternal and infantcharacteristics. Cold stress did not increase the odds of morbidity ordeath. Moderate hypothermia was associated with increased odds of

Severe<32°

Moderate 32-35.9° * Normal36.5-37.9°

Fever≥38°

* Cold Stress 36.0-36.5°

Per

cen

t

Temperature at Admission to NICU (degrees centigrade)

35

30

25

20

15

10

5

31.5 32 32.5 33 33.5 34 34.5 35 35.5 36 36.5 37 37.5 38 38.5 39 39.531 400

Figure 1 Distribution of admission temperatures from the delivery room for 8782 very low birth weight infants born in California neonatal intensive care units.


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IVH and death, and severe hypothermia was associated withincreased odds of death. Severe hypothermia may in fact have agreater impact on morbidity; however, given the small number ofinfants with severe hypothermia (n¼ 9), these associations maynot have been detected.

Maintaining infant normothermia has been shown to improvesurvival and outcomes for decades.7–9 In previous studies,hypothermia has been associated with increased neonatalmorbidity and mortality, such as IVH and death, and to have anincreased association with lower GA in premature infants at the

Table 1 Descriptive characteristics and study demographics

Characteristic N % of total cohort Normothermic (%) Cold stress (%) Moderate/severe (%)

Maternal age (in years)

<20 837 9.5 8.5 9.6 11.2

20–29 3655 41.7 42.6 40.5 41.5

30–39 3727 42.5 42.7 43.1 41.4

X40 554 6.3 6.2 6.8 5.9

Race

Black 1181 13.5 12.1 14.3 14.8

Hispanic White 2537 28.9 29.3 28.9 28.7

Non-Hispanic White 2412 27.5 28.9 27.3 24.8

Asian 948 10.8 10.3 11.2 11.1

Other/unknown 1704 19.4 19.4 18.3 20.5

No prenatal care 375 4.3 4.1 4.4 4.5

Maternal hypertension 2425 28.7 24.6 31.9 32.4

Maternal infection 418 6.0 4.7 5.0 4.9

Uterine infection 505 6.0 7.1 4.9 4.4

Vaginal delivery 2142 24.5 27.2 22.0 22.5

Cesarean section 6603 75.5 72.8 78.0 77.5

Singleton birth 6216 70.8 68.9 72.4 72.2

Multiple birth 2561 29.2 31.1 27.6 27.8

Gender

Female 4452 50.7 50.6 49.3 52.3

Male 4327 49.3 49.4 50.7 47.7

Apgar score: 1 min

0–6 4478 51.1 46.5 49.8 59.6

7–10 4289 48.9 53.5 50.2 40.4

Apgar score: 5 min

0–6 1558 17.8 14.3 15.4 26.3

7–10 7208 82.2 85.7 84.6 73.7

Resuscitation

0 (None) 560 6.4 6.7 6.5 5.9

1 (Blow by O2) 1316 15.0 15.7 17.6 10.9

2 (Continuous positive airway pressure) 1034 11.8 13.7 12.2 8.1

3 (Bag-mask ventilation) 1370 15.6 15.4 17.0 14.4

4 (Endotracheal intubation) 3901 44.4 44.9 41.6 48.1

5 (Chest compressions) 293 3.3 2.5 3.1 4.9

6 (Epinephrine given) 308 3.5 2.1 2.0 7.7

Antenatal steroids 6966 80.1 82.6 79.9 76.3

Spontaneous labor 5278 60.5 63.7 57.5 58.2

Prolonged rupture of membranes 1382 16.3 18.6 15.0 13.6


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threshold of viability.3,10 Following an initial period of stabilization,LBW infants born in the United States are routinely maintained ina variety of thermoneutral environments. Several studies and

reviews have been carried out to evaluate interventions that maybe valuable in decreasing post-birth heat loss in very preterminfants,11–13 and currently the latest guidelines for newbornresuscitation from the American Academy of Pediatricsemphasize the goal of preventing hypothermia in prematureinfants.14 Despite the emphasis placed on maintainingnormothermia, no population-based investigation of thedistribution and predictors of initial temperatures using WHOcriteria in VLBW infants born in contemporary neonatal intensivecare units and their relationship to morbidity and mortality hasbeen published.

The WHO divides hypothermia into three major categories:severe (<32 1C), moderate (32.0 to 35.9 1C) and mild/cold stress(36.0 to 36.4 1C).6 We used the WHO criteria as it was consideredto provide more clinically relevant benchmarks than defininghypothermia as a dichotomous variable or in single-degreeincrements. For example, if one defines hypothermia as a singlecutoff point of <36.5 1C, one combines cold-stressed infants whoare not at risk for short-term morbidity or death with moderatelyand severely hypothermic infants whose risk for IVH and death issignificantly increased. In addition, the WHO categories are usedworldwide.

Our study using WHO categories also suggests that there is amaturational difference between severe/moderate hypothermia and

Table 2 Risk factors for WHO criteria of moderate/severe hypothermia, cold stress and any hypothermia as determined by logistic regression models

Moderate/severe (95% CL) Cold stress (95% CL) Any low temperature (95% CL)

Birth weight (vs 1400–1499)

1000–1099 g NS 1.3 (1.0–1.6) 1.3 (1.0–1.5)

900–999 g 1.6 (1.3–2.0) 1.3 (1.1–1.6) 1.5 (1.2–1.8)

800–899 g 1.7 (1.3–2.1) NS 1.4 (1.1–1.7)

700–799 g 2.2 (1.7–2.8) 1.3 (1.1–1.7) 1.7 (1.4–2.1)

600–699 g 3.8 (2.9–4.9) 1.6 (1.2–2.1) 2.5 (2.0–3.2)

500–599 g 4.2 (3.1–5.9) 1.8 (1.2–2.5) 2.9 (2.1–3.8)

400–499 g 8.0 (4.2–15.3) 2.6 (1.3–5.3) 5.0 (2.7–9.3)

Delivery mode (Cesarean vs vaginal) 1.2 (1.0–1.4) 1.3 (1.1–1.5) 1.2 (1.1–1.4)

Spontaneous labor 0.8 (0.7–0.9)a 0.9 (0.8–1.0)a 0.8 (0.8–0.9)a

Prolonged rupture of membranes 0.7 (0.6–0.9)a 0.8 (0.7–0.9)a 0.8 (0.7–0.9)a

Antenatal steroids 0.7 (0.6–0.8)a 0.9 (0.8–1.0)a 0.8 (0.7–0.9)a

Maternal hypertension 1.1 (1.0–1.1) NS NS

1 min Apgar (0–6 vs 7–10) 1.1 (1.0–1.3) 1.1 (1.0–1.3) 1.1 (1.0–1.3)

5 min Apgar (0–6 vs 7–10) 1.5 (1.3–1.7) NS 1.3 (1.1–1.4)

Resuscitation (none vs any in delivery room) NS 0.8 (0.7–0.9)a 0.8 (0.7–0.9)a

Multiple gestation NS 0.8 (0.7–0.9)a 0.9 (0.8–1.0)a

Race

Black 1.3 (1.1–1.5) NS 1.2 (1.1–1.4)

Asian NS NS 1.2 (1.0–1.4)

Abbreviations: CL, confidence limits; NS, not statistically significant; WHO, World Health Organization.aRepresents factors associated with lower risk of hypothermia.All odds ratios listed in the table have P<0.05.

Table 3 Neonatal outcomes evaluated according to WHO criteria forhypothermia using bivariate analyses

Morbidity Normal (%)

(N¼ 2233)a

Cold stress (%)

(N¼ 2639)a

Severe/moderate (%)

(N¼ 3740)a

P-value

Stage 3 or 4

ROP

6.5 6.5 11.2 <0.0001

NEC 7.3 7.2 8.8 0.11

Sepsis (early) 2.4 2.0 2.3 0.46

Sepsis (late) 11.4 10.9 15.0 <0.0002

Oxygen at 36

weeks

8.4 6.5 7.0 <0.0001

IVH 6.8 7.0 13.0 <0.0001

Death 6.7 8.5 17.0 <0.0001

Death + IVH

3–4

11.1 12.3 22.8 <0.0001

Abbreviations: IVH, intraventricular hemorrhage; NEC, necrotizing enterocolitis;ROP, retinopathy of prematurity; WHO, World Health Organization.aInfants excluded if they died and did not have the condition.The independent variable is hypothermia. The (%) is the percent of infants in eachsubcohort that have the condition.


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cold stress. As an infant matures in size and gestation, the odds ofbeing severely/moderately cold and at high risk for IVH and deathdecreased, whereas the risk for being cold stressed without anincreased risk for death or short-term morbidity increased. Ataround 26 weeks of gestation and/or at 900 to 1000 g, the odds forhypothermia stabilized, indicating that perhaps a critical point inthe ability to thermoregulate had been reached (Appendix FiguresA1 and A2).

Maternal factors such as Cesarean delivery and hypertensioncarried higher odds of moderate/severe hypothermia, whereasspontaneous labor, PROM and antenatal steroid administrationshowed decreased odds of developing moderate/severe hypothermia,independent of birth weight. Cesarean delivery may contribute tohypothermia as operating rooms are often kept at coolertemperatures for the physician’s comfort. The WHO hasrecommended that delivery or resuscitation room temperatures beset at a minimum of 25 1C (771 F), with a suggested range of 25 to28 1C (77 to 82.4 1F),6 which anecdotally is often not the case.Infant characteristics that were associated with hypothermia mostnotably included decreasing birth weight and low Apgar scores.Prematurity and LBW are associated with a large surface area-to-body mass ratio, decreased subcutaneous fat, greater body watercontent, immature skin leading to increased evaporative water andheat losses, a poorly developed metabolic mechanism forresponding to thermal stress and delayed development of skinblood-flow control reducing the ability to maintain heat byvasoconstriction,15–17 all of which may lead to hypothermia. LowApgar scores may be associated with increased resuscitative effortsor increased inherent illness in the infant at birth, of whichhypothermia may be a marker or result.

Cold stress was also associated with LBW, Cesareansection and a low 1-min Apgar score. Decreased odds ofhypothermia were found for spontaneous labor, PROM andantenatal steroid use, as well as for no resuscitative efforts in thedelivery room and multiple gestation. We speculate thatthe reason for no resuscitative effort being associated withnormothermia may be due to the likelihood that a lack ofresuscitation may indicate that the infant was relatively healthierand therefore was able to better maintain core body temperature.In addition, in the midst of resuscitation, measures to keep infantswarm may be difficult to maintain or neglected altogether.Although cold stress was not found to be associated with short-termmorbidities, the long-term consequences of mild hypothermiaremain unknown.

Neonatal outcomes were evaluated and support previous studiesthat showed an association between hypothermia and IVH anddeath.1–3 Our study revealed higher odds of IVH with moderatehypothermia and higher odds of death with both severe andmoderate hypothermia. Despite the association of ROP, oxygen useat 36-week-corrected age and late sepsis with hypothermia onbivariate analyses, in risk adjusted logistic regression models,

hypothermia was not a significant risk factor, likely representingthe confounding effect of factors such as birth weight.

A study by Laptook et al.18 in 2007 evaluated admissiontemperature of LBW infants to determine predictors and associatedmorbidities. The distribution of temperatures was similar to thatfound in our study. Using multivariate analysis, they concludedthat birth weight alone had a relatively small effect onhypothermia. This was in contrast to our results. Their outcomeanalyses revealed an association of admission temperature withdeath and late-onset sepsis, but not with severe IVH.

There were several limitations to our study. The exact timingthat the temperature was obtained within the first hour ofadmission is unknown. A longer time between birth and firstrecorded temperature may result in lower initial temperatures;however, a study by Loughead et al.19 found no significantdifference in the time passed between delivery and initialtemperature with a range of less than 10 min to greater than31 min. The method by which temperature was obtained was alsounknown (rectal, axillary or skin), which may lead to differencesin reported temperatures.

Insights gained from this study have the potential to facilitatequality improvement efforts both in California and nationwide.This study revealed that using the WHO criteria for hypothermia isa valuable method for evaluating infants at the greatest risk fordeveloping low temperatures and for those at greatest risk for pooroutcomes because of hypothermia. In our California cohort, 25.8%of VLBW infants were at increased risk of mortality because ofmoderate/severe hypothermia following birth. A review of the ratesof moderate/severe hypothermia by the CPQCC center shows a widevariation in the percentage of VLBW infants found to behypothermic, ranging from less than 5% to greater than 70%(details available on request). We suspect that this high variabilitymay be widespread in developed countries, making reduction in thepercentage of infants with moderate-to-severe hypothermia ahigh priority for quality improvement initiatives. A variety ofinterventions, such as polyethylene bags, heating mattresses orincreasing the delivery room temperature, have been shown toreduce hypothermia in premature infants, both in randomizedtrials and in quality improvement projects.20–22 Because of itsrelationship to IVH and neonatal mortality, we believe that changein the percentage of moderate/severe hypothermia as defined byWHO may serve as an important indicator of the effectiveness ofone’s interventions. Future studies could then focus on comparisondata before and after any recommended practice changes areimplemented to evaluate for effectiveness in improving neonatalhypothermia and outcomes.

Conflict of interest

The authors declare no conflict of interest.


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Acknowledgments

This project was supported in part by NIH/NCRR/OD UCSF-CTSI Grant Number

KL2 RR024130. Its contents are solely the responsibility of the authors and do not

necessarily represent the official views of the NIH.

References

1 Mathur NB, Krishnamurthy S, Mishra TK. Evaluation of WHO classification of

hypothermia in sick extramural neonates as predictor of fatality. J Trop Pediatr 2005;

51: 341–345.

2 Daga AS, Daga SR, Patole SK. Determinants of death among admissions to intensive

care unit for newborns. J Trop Pediatr 1991; 37: 53–56.

3 Costeloe K, Hennessy E, Gibson AT, Marlow N, Wilkinson AR. The EPICure study:

outcomes to discharge from hospital for infants born at the threshold of viability.

Pediatrics 2000; 106: 659–671.

4 Yu VY, Joseph R, Bajuk B, Orgill A, Astbury J. Perinatal risk factors for necrotizing

enterocolitis. Arch Dis Child 1984; 59: 430–434.

5 Szymonowicz W, Yu VY, Wilson FE. Antecedents of periventricular haemorrhage in

infants weighing 1250 g or less at birth. Arch Dis Child 1984; 59: 13–17.

6 Organization WH. Thermal Protection of the Newborn: A Practical Guide. Geneva:

Switzerland, 1993.

7 Silverman WA, Balnc WA. The effect of humidity on survival of newly born premature

infants. Pediatrics 1957; 20: 477–486.

8 Silverman WA, Fertig JW, Berger AP. The influence of the thermal environment upon

the survival of newly born premature infants. Pediatrics 1958; 22: 876–886.

9 Buetow KC, Klein SW. Effect of maintenance of ‘normal’ skin temperature on survival

of infants of low birth weight. Pediatrics 1964; 34: 163–170.

10 Dincsoy MY, Siddiq F, Kim YM. Intracranial hemorrhage in hypothermic low-birth-

weight neonates. Child’s Nerv Syst. 1990; 6: 245–248; discussion 248.

11 Watkinson M. Temperature control of premature infants in the delivery room. Clin

Perinatol 2006; 33: 43–53, vi.

12 Vohra S, Roberts RS, Zhang B, Janes M, Schmidt B. Heat Loss Prevention (HeLP) in the

delivery room: a randomized controlled trial of polyethylene occlusive skin wrapping in

very preterm infants. JPediatr 2004; 145: 750–753.

13 Sedin G. To avoid heat loss in very preterm infants. J Pediatr 2004; 145: 720–722.

14 Pediatrics AAP. Textbook of Neonatal Resuscitation. 2006: 8–6.

15 Aylott M. The neonatal energy triangle. Part2: thermoregulatory and respiratory

adaption. Paediatr Nurs 2006; 18: 38–42.

16 Hammarlund K, Sedin G. Transepidermal water loss in newborn infants. VI. Heat

exchange with the environment in relation to gestational age. Acta Paediatr Scand

1982; 71: 191–196.

17 Costarino A, Baumgart S. Modern fluid and electrolyte management of the critically ill

premature infant. Pediatr Clin North Am 1986; 33: 153–178.

18 Laptook AR, Salhab W, Bhaskar B. Admission temperature of low birth weight infants:

predictors and associated morbidities. Pediatrics 2007; 119: e643–e649.

19 Loughead MK, Loughead JL, Reinhart MJ. Incidence and physiologic

characteristics of hypothermia in the very low birth weight infant. Pediatr Nurs 1997;

23: 11–15.

20 Bhatt DR, White R, Martin G, Van Marter LJ, Finer N, Goldsmith JP et al. Transitional

hypothermia in preterm newborns. J Perinatol 2007; 27(Suppl 2): S45–S47.

21 McCall EM, Alderdice FA, Halliday HL, Jenkins JG, Vohra S. Interventions to prevent

hypothermia at birth in preterm and/or low birth weight infants. Cochrane Database

Syst Rev 2008; (2): CD004210.

22 Lee HC, Ho QT, Rhine WD. A quality improvement project to improve

admission temperatures in very low birth weight infants. J Perinatol 2008; 28:

754–758.

Table A1 Admission temperature for infants <32 weeks gestational age withbirth weight <1500 g by gestational age

Gestational

age (weeks)

N Mean BW

(s.d.)

Mean temp

(s.d.)

Range

23 263 606 (90) 35.3 (1.3) 31.0–38.4

24 572 672 (103 35.8 (1.2) 26.1–39.0

25 732 762 (128) 36.1 (0.9) 32.8–39.5

26 820 876 (160) 36.3 (0.8) 32.2–39.2

27 993 978 (180) 36.3 (0.7) 32.3–39.1

28 1120 1097 (204) 36.4 (0.8) 27.0–39.2

29 1311 1195 (198) 36.4 (0.7) 26.1–38.6

30 1022 1245 (185) 36.4 (0.7) 33.4–39.1

31 413 1295 (169) 36.3 (0.6) 33.0–37.9

32 235 1310 (149) 36.3 (0.6) 34.8–38.0

Abbreviation: BW, birth weight.

Table A2 Admission temperature for infants <32 weeks gestational age withbirth weight <1500 g by birth weight

Birth weight (g) N Mean GA (s.d.) Mean temp (s.d.) Range

400–499 87 24.7 (1.7) 35.4 (1.3) 32.0–39.1

500–599 343 24.5 (1.6) 35.6 (1.1) 31.7–38.3

600–699 622 25.0 (1.8) 35.8 (1.1) 30.5–39.0

700–799 793 25.7 (1.8) 36.1 (1.0) 26.1–39.5

800–899 800 26.6 (1.8) 36.3 (0.7) 33.1–38.5

900–999 792 27.4 (1.8) 36.2 (0.7) 32.9–39.0

1000–1099 905 28.2 (1.9) 36.4 (0.8) 26.7–39.2

1100–1199 973 29.1 (1.9) 36.4 (0.7) 33.2–38.6

1200–1299 1076 29.8 (1.9) 36.4 (0.7) 27.0–39.1

1300–1399 1159 30.4 (1.9) 36.4 (0.6) 33.5–38.4

1400–1499 1232 31.1 (1.9) 36.4 (0.7) 26.1–39.6

Abbreviation: GA, gestational age.

Appendix


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80.0

90.0

60.0

70.0

40.0

50.0

Per

cen

tag

e

Gestational Age (weeks)

20.0

30.0

0.0

10.0

23 24 25 26 27 28 29 30 31 32

Moderate/Severe

Cold Stress

Total Cold

Figure A1 Percentage of hypothermia by gestational age. The total number of cold infants is divided into WHO temperature categories of moderate/severe hypothermiaand cold stress.

Percentage of Hypothermia by Birth Weight

80

90

50

60

70

30

40

Per

cen

tag

e

10

20

0

Birth weight (grams)

Moderate/SevereCold stress

Total cold

Figure A2 Percentage of hypothermia by birth weight. The total number of cold infants is divided into WHO temperature categories of moderate/severe hypothermia andcold stress.


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