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Society for Obstetric Anesthesia and Perinatology

Section Editor: Cynthia A. Wong

The Incidence and Prevention of Hypothermia
in Newborn Bonding after Cesarean Delivery:
A Randomized Controlled Trial
Ernst-Peter Horn, MD,* Berthold Bein, MD,† Markus Steinfath, MD,†
Kerstin Ramaker, MD,‡ Birgit Buchloh,‡ and Jan Höcker, MD†

BACKGROUND: Little is known about thermoregulation of the newborn while bonding on the
mother’s chest immediately after cesarean delivery. Newborn hypothermia is associated with
serious complications and should be avoided. Therefore, we evaluated whether newborns
develop hypothermia during intraoperative bonding while positioned on their mothers’ chests
and investigated the effects of active cutaneous warming of the mothers and babies during a
20-minute intraoperative bonding period.
METHODS: We enrolled 40 parturients scheduled for elective cesarean delivery under spinal
anesthesia. Mothers and their newborns were randomized to receive either passive insulation
or forced-air skin-surface warming during the surgical procedure and bonding period. The pri-
mary outcome was neonatal core temperature at the end of the bonding period. Core tempera-
tures of the newborns were measured with a rectal probe. Body temperatures of the mothers
were assessed by sublingual measurements. Skin temperatures, thermal comfort of the moth-
ers, and perioperative shivering were evaluated.
RESULTS: Without active warming from the beginning of the surgical procedure until the end
of the bonding period, the mean (SD) neonatal core temperature decreased to 35.9 (0.6)°C.
Seventeen of 21 (81%) newborns became hypothermic (defined as a core temperature below
36.5°C). Active skin-surface warming from the beginning of the surgical procedure until the end
of the bonding period resulted in a neonatal core temperature of 37.0 (0.2)°C and a decreased
incidence of hypothermia (1 of 19 (5%) newborns (P < 0.0001)). In addition, active warming
increased the mean skin temperatures of the infants, maternal core and skin temperatures,
maternal thermal comfort, and reduced perioperative shivering.
CONCLUSIONS: Active forced-air warming of mothers and newborns immediately after cesarean
delivery reduces the incidence of infant and maternal hypothermia and maternal shivering, and
increases maternal comfort.  (Anesth Analg 2014;118:997–1002)

H
ypothermia in newborns is common with a global hypothermia is usually not a direct cause of death, it contrib-
prevalence up to 85% in hospitals and up to 92% at utes to mortality caused by conditions such as severe infec-
home.1 “Normal” temperature at birth is between tion, prematurity, and asphyxia1 as well as intraventricular
36.5°C and 37.5°C with a tendency to lower values after hemorrhage.7,8
cesarean delivery.2 Neonatal hypothermia is commonly There are several approaches and devices for prevention
defined as a core temperature below 36.5°C.2–5 Hypothermia and treatment of newborn hypothermia such as warming
contributes to neonatal mortality and morbidity, espe- mattresses, plastic wraps, bags, and caps.5,9 In addition,
cially in preterm and low birth weight infants.6 Although skin-to-skin care on the mother’s chest compared with
conventional incubator care is effective in reducing the
risk of neonatal hypothermia.5 This position is described
From the *Departments of Anesthesiology and Intensive Care Medicine, Re-
gio Klinikum Pinneberg, Pinneberg, Germany; †Department of Anesthesiol- as the bonding position and can be held until the infant
ogy and Intensive Care Medicine, University Hospital Schleswig-Holstein, latches onto the breast for the first feeding. A close bond
Campus Kiel, Kiel, Germany; and ‡Department of Gynecology and Obstet-
rics, Regio Klinikum Pinneberg, Pinneberg, Germany. between the mother and her newborn is essential for a 
Accepted for publication December 9, 2013. close relationship and adequate growth of the infant and is
Funding: This study was funded by the Department of Anesthesiology and actively promoted by midwives during the first half-hour
Intensive Care Medicine, University Hospital Schleswig-Holstein, Campus after delivery.10,11 After vaginal delivery outside the oper-
Kiel, Kiel, Germany.
ating room, skin-to-skin bonding of the newborn appears
The authors declare no conflicts of interest.
safe about thermoregulatory disorders. For example, even
This report was previously presented, in part, at the 60. Deutscher Anaesthesie
Congress (DAC), Nuernberg, Germany, April 20–22, 2013. in preterm infants, 1 hour of skin-to-skin bonding was not
Reprints will not be available from the authors. associated with hypothermia compared with those infants
Address correspondence to Jan Höcker, MD, Department of Anesthesiology placed in an incubator.12
and Intensive Care Medicine, University Hospital Schleswig-Holstein, Cam- Today, healthy parturients undergoing cesarean delivery
pus Kiel, Kiel, Germany, Schwanenweg 21, 24105 Kiel, Germany. Address
e-mail to jan.hoecker@uksh.de.
are awake during surgery, because neuraxial anesthesia is
Copyright © 2014 International Anesthesia Research Society the standard of care in the developed world. The thermal
DOI: 10.1213/ANE.0000000000000160 outcome of the newborn who bonds on the mother’s chest

May 2014 • Volume 118 • Number 5 www.anesthesia-analgesia.org 997

end of surgery. and an infusion of and assessing 1. exclusion criteria were any expected warmer (Smiths Medicals. Jan Höcker). Luebeck. After the baby was born.and 5-minute Apgar scores. Smiths Medicals. M. midwives assessed and cared for the newborn on an 37°C Approximately. The was maintained near 23°C. Allocated to receive active warming Allocated to receive passive insulation (n = 19) (n = 21) Lost to follow-up (n = 0) Lost to follow-up (n = 0) Analyzed (n = 19) Analyzed (n = 21) 998    www. A 25-gauge spinal needle was inserted between the Schwanenweg 20. flipping a coin. Just before initiating spinal babies versus passive insulation during the intraoperative anesthesia. second and third (L2-L3) or the third and fourth (L3-L4) Dr. If the 5-minute Ringer’s solution was started at a rate of 500 mL/h until Apgar score was ≥9 and the newborn was deemed stable. Participant Consolidated Standards of Reporting Trials flow diagram. we randomized 40 nal anesthesia was established. Principal investigator: PD fluid 1.5% and 5 μg Dr. cardiotocography. All fluids were at room temperature. patients arrived at the delivery ward Germany) for the first 5 minutes of life by drying the baby where a venous cannula was inserted. of cesarean delivery. Parturients did not receive all women scheduled for planned cesarean delivery under any IV opioids. chorioamnionitis.gov on February 12. spinal anesthesia in our clinic were asked to participate in In the active warming group. patients were covered by prewarmed cot- amniotic fluid. 1). and The cesarean delivery began soon after adequate spi- after obtaining written informed consent. tiation of anesthesia until the end of the surgical procedure. We identified 63 eligible parturients. spinal space was identified by free flow of cerebrospinal 2013 (Identifier: NCT01793558. than 18 years. (=1 mL) sufentanil as injected slowly with the goal of During a 6-week period between February and April 2013. Intraoperative ambient temperature mother’s chest immediately after cesarean delivery. This study was approved by the IRB (University Kiel. meconium-stained insulation group. 60 minutes before the expected start warm newborn table (Babytherm 8000. Germany. Mehdorn) on February 14. H. placenta previa or abruption. MA) was set to “high problems with the newborn such as week of gestation <36 level” (44°C) during the warming period. In the passive or >42. Patients he/she was positioned naked (the infant head was routinely Assessed for eligibility (n = 63) Excluded (n = 23) ♦ Declinedto participate (n = 18) ♦ Received general anesthesia (n = 1) ♦ Cesarean delivery not carried out (n = 4) Randomized (n = 40) Figure 1. When the and registered with ClinicalTrials.6 mL hyperbaric bupivacaine 0. A Level 1 Equator® anesthesia. or if cesarean delivery was planned under general patient laying on the operating table. or any abnormalities in ton blankets taken from a 40°C heating cabinet. In addition. Chairperson: Prof. a forced-air cover (Level the study.anesthesia-analgesia. 2012 (No: A 138/11) interspace with the patient in sitting position. 2 treatment groups: passive insulation (no active warming) trolled trial. All operations were performed effects of active cutaneous warming of the mothers and in a single operating room. 24105 Kiel. parturients for study participation (Fig. MA) was positioned over the upper body of the or higher. classified as American ASA physical status III Rockland.org anesthesia & analgesia . The primary outcome was the neonatal core or active forced-air warming starting immediately after ini- temperature at the end of the bonding period. Rockland. Parturients were excluded if they were younger 1 Snuggle Warm® Upper Body Blanket. Dräger.Hypothermia in Newborns Bonding after Cesarean Delivery immediately after delivery in the operating room has not were prepared for cesarean delivery that included receiving been systematically investigated. the aim of our study was to evaluate whether eratively and were then transported into the central surgi- the newborn becomes hypothermic when bonding on the cal area of the hospital. patients were randomly assigned to one of the bonding process were evaluated in this randomized con. Randomization was performed by a nurse not involved in METHODS the study. 30 mL sodium citrate oral premedication 20 minutes preop- Therefore.4 to 1. achieving a sensory level of T4.

CA) and R 2. Exergen Corporation. San Diego. low-intensity shiv- ering. We followed Active warming of the mothers was stopped. If babies showed any Computing. babies were sepa. Watertown. by the midwives after the end of the bonding period. Ostend. Model Dermatemp temperature. Morphometric maternal characteristics and room temper- Mean skin temperature was calculated from these measure. assessed simultaneously on the chest at the start of surgery. bradycardia. the probe was removed. In the passively insulated group. All 40 subjects completed the study protocol without any skin temperatures were measured (Infrared Temperature dropouts. and heart rate were first nea.16 Data are expressed as mean (SD) after the end of the surgical procedure. thigh. P < 0. The babies remained carefully covered in this tics software GraphPad Prism 5.75 in both groups) on babies’ core temperatures Figure 2. mothers generally reported a comfortable warm feeling.05. Assumptions the cotton blanked in the passive insulation group or under were based on a previous study from our group. Rockland. 3 = continuous.14 the forced-air cover in the actively warmed group (Fig.5°C. Model 2080. heart rate. Boeblingen. observation period (data not shown). or rectal temperature below 35. Peripheral oxygen satura- vital disturbances such as asphyxia. a rectal temperature probe was considered significant. and the babies were actively warmed subsequently averaged among the mothers in each group. 20-minute bonding period. ature were not different between groups (Table  1). bradyp. tion.0 (R® Foundation for Statistical the midwife and the anesthesiologist. ture was not different between groups at the start of the surement. Maternal core tempera- sublingual pocket by lifting the tongue. MA) was skin temperatures at the beginning and the end of bonding May 2014 • Volume 118 • Number 5 www. maternal DT-1001.11. arm. nor did it differ from baseline ture (Infrared Temperature Scanner. Exergen Corporation. Shivering of the mother was graded by the investiga- tor at start of the cesarean delivery and the beginning and the end of the 20-minute bonding period by using a 4-point scale (0 = no shivering.2–5 Sample size calculation for the study was performed by using MedCalc for Windows 12. Boeblingen. Continuous. Upper Body Blanket.05 was Directly after birth. Thermal comfort of the mother was evaluated with a 100-mm visual analog scale with 3 anchored definitions: −50 mm was defined as “worst imaginable cold. The babies the method of Diehr et al.5°C (SD 0. Philips. rated from the mother and placed on the newborn table for Differences between the groups were compared with χ2 tests approximately 2 minutes to measure skin temperatures. normally distributed variables were analyzed After the 20-minute bonding period. respectively. Vienna. was estimated to provide 80% power for detecting a statistically significant difference covered with a cotton cap) on the chest of the mother under between study groups at an α level of 0. by the midwife or pediatrician. and mean arterial start of the cesarean delivery and the beginning and the end blood pressures did not differ between groups during the of the 20-minute bonding period. Bonding a neonate on the chest of the mother in the active warming group by using a forced-air cover (Level 1 Snuggle Warm® at the end of the bonding period. All newborns were stable at 5 minutes and could be placed Peripheral oxygen saturation. inserted into the newborn and connected to a moni- tor (IntelliVue MP50.. 21 parturients were randomized to the treat- Scanner. Maternal skin tempera. 1 = intermittent.org 999 . start of bonding. 2 = moderate shivering. Germany) of the mothers were recorded and compared at Peripheral oxygen saturation. Philips. Mother and baby left the operating room directly with changes over time. MA).5® (MedCalc Software. hypothermia was defined as a maternal core temperature of < 36°C and a neonatal core temperature <36. Germany) for RESULTS continuous core temperature assessment. maternal core and sublingual temperature probe (Temp-Plus II. and after 20 minutes of bonding. A sample size of 40 subjects. Spinal ments. on the mother’s chest. rial blood pressure (IntelliVue MP50. In addition. intense shiv- ering). 20-minute bonding period at chest. and 19 parturients were Watertown. including 10% (n  =  4) dropouts.anesthesia-analgesia.” 0 mm as “thermally neutral. and calf. Maternal core temperature was assessed by placing a At the start of the cesarean delivery. Belgium) and based on an expected treatment effect of 0. or median (interquartile range). the bonding was averaged over time for each mother. position for a 20-minute period of bonding observed by San Diego. MA) 5 minutes after birth and at the end of the randomized to the control (passive insulation) group. Austria). mean arterial blood pressure. Statistical analyses were performed by using statis- respectively. and with paired and unpaired Student t test. These values were stopped immediately. Smiths Medicals. ment (active warming) group. CA) into the posterior ferent between groups (Table  2).” and +50 mm as “insufferably hot. skin temperatures and the thermal comfort were not dif- Alaris™.0® (GraphPad Software. heart rate. Model Dermatemp DT-1001.” In accordance with current guidelines and other studies. After each mea. and mean arte.15 to increase statistical power by were clothed and positioned again on the chest of the performing an unmatched analysis of the matched data mother. Carefusion. Active warming was well tolerated.13 Length and weight of the newborn were assessed anesthesia was successfully performed in all parturients. by using 1-way analysis of variance and Scheffé’s F test.0°C. 2).

5 (0. Room temperature was measured by electronic thermometry.0007 Skin temperature at start of surgery (°C) 33. sive warming during skin-to-skin bonding on the mother’s ing period.2)°C in actively warmed tures.5) 36.0008 b <0. core chest during cesarean delivery. mean (SD) rectal temperature of passively insulated of the infants and their mothers’ core and skin tempera- babies was 35. maternal core and skin warmed versus passively insulated infants (33. Both paired and unpaired analysis15. (n = 19) Age (y)a 31 (6) 31 (5) Maternal weight (kg)a 90 (22) 90 (16) Maternal height (cm)a 165 (7) 166 (7) Maternal body mass index (kg/m2)a 33.0001).3)°C) temperatures and thermal comfort were significantly higher (Fig. age did not differ between groups.0001 b 0. active warming. core temperatures from baseline to the end of the 20-minute Length and weight of the newborns and the gestational bonding period were P < 0.anesthesia-analgesia.3 (0. 5 minutes after birth.4 (1. no warming.4 (0. (48%).9 (0.8)ab 0.5)°C in actively At the end of the bonding period.0007).6)°C vs 37. a Versus temperature at start of surgery.  3). 1000    www. starting immediately after the establish- of babies in the passive warming group was significantly ment of the spinal block and continued during the bonding lower than babies with active warming at 5.3 (1.9 (1.1 (2.5) Core temperature at start of bonding (°C) 36.7)ab a 0.0001 Thermal comfort at start of surgery (mm) −4 (8) 0 (9) Thermal comfort at start of bonding (mm) −6 (9) 2 (12)b b 0.4) Skin temperature at start of bonding (°C) 33. Intermittent low-intensity shivering (grade 1) was pres- out active warming. and perioperative shiv- babies (P < 0. At the end of the bonding addition.5)a 36. Neonatal. Hypothermia was present in 17 of 21 ering was reduced in actively warmed mothers.2 (7.1 (0. 15 and period. active warming increased mean skin temperature period.2) Extension of the spinal block (level)b T 4 (T4-T5 [T4-T5]) T 4 (T4-T5 [T3-T5]) Neonatal gestational age (weeks)a 38 (1) 38 (2) Neonatal weight (g)a 3319 (291) 3533 (448) Neonatal length (cm)a 51. caw Versus value at start of surgery. b Data are presented as median (IQR [range]). prevented hypothermia in 95% of the newborns. (81%) of the passively warmed and in 1 of 19 (5%) of the trast. In con. Maternal Temperature Assessments and Thermal Comfort Group. 4). However.7) a Data are presented as mean (SD). it was significantly higher 35.0 (0. Soon after the start of the bonding period.0001). cnw Versus value at start of surgery. ent in 5 of 21 (24%) of the passively insulated and in none of ers became hypothermic at the end of the bonding period the actively warmed parturients (P < 0.9 (0.4 (0.3 (1. warming. group no warming. skin temperature actively warmed babies (P < 0. Immediately after birth. b Versus no warming.0 (0. Active cutaneous warming temperature decreased in both groups.009 caw 0.5) 36.4 (0. Table 2. borns became hypothermic if they received standard pas- after 1 and 5 minutes. in actively warmed mothers compared with mothers with.8) 35. were not different from baseline skin temperature.0001). in actively warmed parturients. (n = 19) P Core temperature at start of surgery (°C) 36.” and +50 mm as “insufferably hot” visual at the start of the cesarean delivery and at the beginning and the end of the 20-minute bonding period.001 a 0.  Maternal.16 of the neonatal ing group reached hypothermia level (5%) (P = 0.3) Ambient temperature during surgery (°C)a 23. 10. however.014 Thermal comfort after 20 min bonding (mm) −9 (10)c 7 (10)cb b <0.7) 35.8) 52.2 (0. period.8 (1.7 (6.org anesthesia & analgesia . and Environment Characteristics Group. Data are presented as mean (SD).7 (0. No differences in rectal temperature The main finding of our study was that 81% of the new- between groups were detected immediately after birth. throughout bonding was significantly higher compared Mean skin temperature of the infants was not different with baseline skin temperature and to the passively insu.4)b a <0.0001 cnw 0. rectal temperature of the newborns was near 37. the core temperature of the mothers.022 Thermal comfort was evaluated with a 100-mm visual analog scale: −50 mm was defined as “worst imaginable cold.6) 34. (n = 21) Group.0 (0. group active warming. Thermal comfort was higher.5°C in DISCUSSION all neonates (Fig.  3). only 1 of 19 parturients in the active warm.0 (1.” 0 mm as “thermally neutral. (n = 21) Group.8) 22. and at the beginning of the bond.0001. no warming. In 20 minutes of bonding (Fig.0001 b Skin temperature after 20-minute bonding (°C) 32.4) Core temperature after 20-minute bonding (°C) 36.Hypothermia in Newborns Bonding after Cesarean Delivery Table 1.6) 32. at the end of the bonding lated mothers. Ten of the 21 passively insulated moth.

11 Disruptions in maternal–infant bond- ing are correlated with pediatric bronchial asthma and were No warming Active warming Active vs. Detailed P values for of hypothermia is considered one of the most essential ele- active warming versus no warming during bonding period and versus ments of neonatal care.17 especially if they are premature. ing the umbilical cord.22. thigh. However.5 warming alone does not prevent intraoperative hypother- 33 = no warming mia or shivering in women undergoing elective cesarean 32. or are delivered by cesarean delivery. defined as a In our study. and calf.5 = active warming † † † Spontaneous labor.022 0.0001 vs temperature 5 minutes after birth.5 play a role. we planned a 20-minute bonding period core temperature lower than 36.5 = active warming delivery with spinal anesthesia. This “bond- B ing position” of the newborn for the first 30 minutes of life is favored by most midwives to provide close interaction between Time (min) P values bonding mother and her child. Without active cutaneous warming. found to be related to physical separation at birth. †P < 0. sublingual temperature has been demon- cutaneous warming.13 but could be studied as topics of future research. prolonged rupture of membranes. Neonatal mean skin temperature (°C) 5 minutes after birth Lower temperatures. Figure 4. or and after the 20-minute bonding period. Although negative effects (i. it is a common practice to place Time (min) the newborn skin to skin on the mother’s chest.0001 <0.8 35.5 In fact. *P vs no warming. required to finish a cesarean delivery operation after clamp- ate whether the forced-air warming blanket applied dur.0001 <0. and the recommended method nal skin temperature was 2.0001 outside operating rooms but also during cesarean delivery in 10 <0. plas- tic wraps. Forced-air warming systems with temperature at birth. Neonatal rectal temperatures (°C) at birth and during and mortality remain speculative.0001 <0. and † † antenatal steroid administration have been associated with birth 1 min 5 min 0 5 10 15 20 decreased risk of hypothermia. midwives and moth- 0 0. acidosis. Nevertheless.2)°C to 37. Data are presented as mean (SD). other neonatal warming devices. active warming as per.0001 neonates.0001 vs no warming..25 only one of 19 newborns became hypothermic.18 Mothers (versus versus No warming who received extra contact exhibited significantly more affec- temperature at temperature at tionate behavior toward their infants than did the mothers birth) birth who received routine care.0 (0. Further. prevention the 20-minute bonding period. Longer bonding periods would not ing bonding or “prewarming” of maternal skin resulting in have been appropriate because at the end of surgery the May 2014 • Volume 118 • Number 5 www.5°C. close to core temperature. Intraoperative lower body forced-air 34 *† 33.e.0001 <0.0001 <0.0001 <0. To our knowledge. brane temperature24 that reflects the temperature of the core ing bonding from 37.5.org 1001 .0001 <0. we measured rectal temperatures in the newborns strating the rapid decrease of core temperature in newborns and sublingual temperatures in the mothers that might dif- during bonding on the mother’s chest without any active fer from core temperatures. neonates are at high risk for hypothermia.20 35.0001 awake mothers under spinal or epidural anesthesia. However.5 36 maintaining body temperature.0001 <0. Nevertheless. we cannot clearly differenti. effects on morbidity Figure 3. †P vs temperature at birth. However. arm. or caps have been found to be efficient for 36. no randomized trial has investigated 15 <0. and mean neonatal of temperature assessment in infants aged <2 years. hypox- emia) seem likely in this population. but these mechanisms must be investigated in 37 further studies. A 38 higher skin temperatures before skin-to-skin contact miti- † *† *† *† *† gated infant heat loss. have low birth weight or 36 = no warming a low Apgar score.4°C lower. T rectal (°C) 36.19 As a result.0001 the consequences of (mild) hypothermia in mature. bags. mean mater. our data showed that even this air temperature was not able to prevent a decrease in core temperature during bonding. To our knowledge.21 32 Our study may be criticized because the temperature of 5 min 20 min the warm air was set to 44°C during the warming period after birth bonding that may have caused hyperthermia in the newborns. We hypothesize that both factors may 37. strated to provide a high correlation with tympanic mem- formed did not prevent a decrease of core temperature dur. thermal compartment. for practical reasons because this is the average time period Given our study design. A. Mean skin temperature was warming either mother or newborn were not investigated an average of skin temperatures of the chest. Data are presented as mean (SD).anesthesia-analgesia. rectal temperature is warming. a ring-shaped cover as well as warming mattresses. *P < 0.8 bonding After vaginal delivery.5 (0. healthy 20 <0.2)°C.0001 0. B.5 sia14 is performed.23 In temperature approximately was 2°C lower than with active adult patients.06 ers encourage bonding procedures not only after deliveries 5 <0.5 Mothers are also at risk of developing hypothermia dur- T mean skin (°C) 35 ing the procedure even when spinal21 or epidural anesthe- 34. this is the first clinical study demon.

4. Bauer K. Anisfeld E. Acta Paediatr 2005. risk factors and outcomes. Puyol P. White DG.82:128–31 erative measurement of sublingual temperature in comparison 3. Carvalho B.14:1491–504 Attestation: Kerstin Ramaker has seen the original study data. Christensson K. MD. Belsches TC. Hamer DH. Höcker J. analyze the J Perinatol 2011. Miller TR. precision and practicability of periop- delivered infants. rectal. Gottschalk A. Cochrane Database Syst Rev In summary. BMC Med 2013. Chomba E.94:775–7 Name: Berthold Bein. J Pediatr 1997. Horn EP. approved the final manuscript. Leadford AE. [Efficacy of ring-shape cover in active skin surface warming in This manuscript was handled by: Cynthia A. Temperature monitoring and perioperative thermo- sioned by National Institute for Health and Clinical Excellence regulation. Tilly AE. the number of pairs is small. Butwick AJ. with tympanic membrane temperature in awake and anaesthe- tent perioperative hypothermia in adults. Horn EP. 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