Hypothermia in newborns is common with a global prevalence up to 85% in hospitals and up to 92% at home.1 “Normal” temperature at birth is between 36.5°C and 37.5°C with a tendency to lower values after cesarean delivery.2 Neonatal hypothermia is commonly defined as a core temperature below 36.5°C.2–5 Hypothermia contributes to neonatal mortality and morbidity, especially in preterm and low birth weight infants.6 Although hypothermia is usually not a direct cause of death, it contributes to mortality caused by conditions such as severe infection, prematurity, and asphyxia1 as well as intraventricular hemorrhage.7,8
There are several approaches and devices for prevention and treatment of newborn hypothermia such as warming mattresses, plastic wraps, bags, and caps.5,9 In addition, 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 as the bonding position and can be held until the infant latches onto the breast for the first feeding. A close bond between the mother and her newborn is essential for a close relationship and adequate growth of the infant and is actively promoted by midwives during the first half-hour after delivery.10,11 After vaginal delivery outside the operating room, skin-to-skin bonding of the newborn appears safe about thermoregulatory disorders. For example, even in preterm infants, 1 hour of skin-to-skin bonding was not associated with hypothermia compared with those infants placed in an incubator.12
Today, healthy parturients undergoing cesarean delivery are awake during surgery, because neuraxial anesthesia is the standard of care in the developed world. The thermal outcome of the newborn who bonds on the mother’s chest immediately after delivery in the operating room has not been systematically investigated.
Therefore, the aim of our study was to evaluate whether the newborn becomes hypothermic when bonding on the mother’s chest immediately after cesarean delivery. The effects of active cutaneous warming of the mothers and babies versus passive insulation during the intraoperative bonding process were evaluated in this randomized controlled trial. The primary outcome was the neonatal core temperature at the end of the bonding period.
This study was approved by the IRB (University Kiel, Schwanenweg 20, 24105 Kiel, Germany; Chairperson: Prof. Dr. H. M. Mehdorn) on February 14, 2012 (No: A 138/11) and registered with ClinicalTrials.gov on February 12, 2013 (Identifier: NCT01793558, Principal investigator: PD Dr. Jan Höcker).
During a 6-week period between February and April 2013, all women scheduled for planned cesarean delivery under spinal anesthesia in our clinic were asked to participate in the study. Parturients were excluded if they were younger than 18 years, classified as American ASA physical status III or higher, or if cesarean delivery was planned under general anesthesia. In addition, exclusion criteria were any expected problems with the newborn such as week of gestation <36 or >42, placenta previa or abruption, meconium-stained amniotic fluid, chorioamnionitis, or any abnormalities in cardiotocography. We identified 63 eligible parturients, and after obtaining written informed consent, we randomized 40 parturients for study participation (Fig. 1).
Approximately, 60 minutes before the expected start of cesarean delivery, patients arrived at the delivery ward where a venous cannula was inserted, and an infusion of Ringer’s solution was started at a rate of 500 mL/h until end of surgery. All fluids were at room temperature. Patients were prepared for cesarean delivery that included receiving 30 mL sodium citrate oral premedication 20 minutes preoperatively and were then transported into the central surgical area of the hospital. Intraoperative ambient temperature was maintained near 23°C. All operations were performed in a single operating room. Just before initiating spinal anesthesia, patients were randomly assigned to one of the 2 treatment groups: passive insulation (no active warming) or active forced-air warming starting immediately after initiation of anesthesia until the end of the surgical procedure. Randomization was performed by a nurse not involved in the study, flipping a coin.
A 25-gauge spinal needle was inserted between the second and third (L2-L3) or the third and fourth (L3-L4) interspace with the patient in sitting position. When the spinal space was identified by free flow of cerebrospinal fluid 1.4 to 1.6 mL hyperbaric bupivacaine 0.5% and 5 μg (=1 mL) sufentanil as injected slowly with the goal of achieving a sensory level of T4. Parturients did not receive any IV opioids.
In the active warming group, a forced-air cover (Level 1 Snuggle Warm® Upper Body Blanket, Smiths Medicals, Rockland, MA) was positioned over the upper body of the patient laying on the operating table. A Level 1 Equator® warmer (Smiths Medicals, Rockland, MA) was set to “high level” (44°C) during the warming period. In the passive insulation group, patients were covered by prewarmed cotton blankets taken from a 40°C heating cabinet.
The cesarean delivery began soon after adequate spinal anesthesia was established. After the baby was born, midwives assessed and cared for the newborn on an 37°C warm newborn table (Babytherm 8000, Dräger, Luebeck, Germany) for the first 5 minutes of life by drying the baby and assessing 1- and 5-minute Apgar scores. If the 5-minute Apgar score was ≥9 and the newborn was deemed stable, he/she was positioned naked (the infant head was routinely covered with a cotton cap) on the chest of the mother under the cotton blanked in the passive insulation group or under the forced-air cover in the actively warmed group (Fig. 2), respectively. The babies remained carefully covered in this position for a 20-minute period of bonding observed by the midwife and the anesthesiologist. If babies showed any vital disturbances such as asphyxia, bradycardia, bradypnea, or rectal temperature below 35.0°C, the bonding was stopped immediately, and the babies were actively warmed by the midwife or pediatrician.
After the 20-minute bonding period, babies were separated from the mother and placed on the newborn table for approximately 2 minutes to measure skin temperatures. Active warming of the mothers was stopped. The babies were clothed and positioned again on the chest of the mother. Mother and baby left the operating room directly after the end of the surgical procedure.
Directly after birth, a rectal temperature probe was inserted into the newborn and connected to a monitor (IntelliVue MP50; Philips, Boeblingen, Germany) for continuous core temperature assessment. In addition, skin temperatures were measured (Infrared Temperature Scanner, Model Dermatemp DT-1001, Exergen Corporation, Watertown, MA) 5 minutes after birth and at the end of the 20-minute bonding period at chest, arm, thigh, and calf. Mean skin temperature was calculated from these measurements.13 Length and weight of the newborn were assessed by the midwives after the end of the bonding period.
Peripheral oxygen saturation, heart rate, and mean arterial blood pressure (IntelliVue MP50; Philips, Boeblingen, Germany) of the mothers were recorded and compared at start of the cesarean delivery and the beginning and the end of the 20-minute bonding period.
Maternal core temperature was assessed by placing a sublingual temperature probe (Temp-Plus II, Model 2080, Alaris™; Carefusion, San Diego, CA) into the posterior sublingual pocket by lifting the tongue. After each measurement, the probe was removed. Maternal skin temperature (Infrared Temperature Scanner, Model Dermatemp DT-1001, Exergen Corporation, Watertown, MA) was assessed simultaneously on the chest at the start of surgery, start of bonding, and after 20 minutes of bonding.
Shivering of the mother was graded by the investigator 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; 1 = intermittent, low-intensity shivering; 2 = moderate shivering; 3 = continuous, intense shivering). 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,” 0 mm as “thermally neutral,” and +50 mm as “insufferably hot.”
In accordance with current guidelines and other studies, hypothermia was defined as a maternal core temperature of < 36°C and a neonatal core temperature <36.5°C.2–5
Sample size calculation for the study was performed by using MedCalc for Windows 12.5® (MedCalc Software, Ostend, Belgium) and based on an expected treatment effect of 0.5°C (SD 0.75 in both groups) on babies’ core temperatures at the end of the bonding period. A sample size of 40 subjects, including 10% (n = 4) dropouts, was estimated to provide 80% power for detecting a statistically significant difference between study groups at an α level of 0.05. Assumptions were based on a previous study from our group.14
Statistical analyses were performed by using statistics software GraphPad Prism 5.0® (GraphPad Software, San Diego, CA) and R 2.11.0 (R® Foundation for Statistical Computing, Vienna, Austria). Peripheral oxygen saturation, mean arterial blood pressure, and heart rate were first averaged over time for each mother. These values were subsequently averaged among the mothers in each group. Continuous, normally distributed variables were analyzed by using 1-way analysis of variance and Scheffé’s F test. Differences between the groups were compared with χ2 tests and with paired and unpaired Student t test. We followed the method of Diehr et al.15 to increase statistical power by performing an unmatched analysis of the matched data with changes over time.,16 Data are expressed as mean (SD) or median (interquartile range), respectively. P < 0.05 was considered significant.
All 40 subjects completed the study protocol without any dropouts; 21 parturients were randomized to the treatment (active warming) group, and 19 parturients were randomized to the control (passive insulation) group. Morphometric maternal characteristics and room temperature were not different between groups (Table 1). Spinal anesthesia was successfully performed in all parturients. All newborns were stable at 5 minutes and could be placed on the mother’s chest. Active warming was well tolerated; mothers generally reported a comfortable warm feeling. Peripheral oxygen saturation, heart rate, and mean arterial blood pressures did not differ between groups during the observation period (data not shown).
At the start of the cesarean delivery, maternal core and skin temperatures and the thermal comfort were not different between groups (Table 2). Maternal core temperature was not different between groups at the start of the 20-minute bonding period, nor did it differ from baseline temperature. In the passively insulated group, maternal skin temperatures at the beginning and the end of bonding were not different from baseline skin temperature. In contrast, in actively warmed parturients, skin temperature throughout bonding was significantly higher compared with baseline skin temperature and to the passively insulated mothers.
At the end of the bonding period, maternal core and skin temperatures and thermal comfort were significantly higher in actively warmed mothers compared with mothers without active warming. Ten of the 21 passively insulated mothers became hypothermic at the end of the bonding period (48%); however, only 1 of 19 parturients in the active warming group reached hypothermia level (5%) (P = 0.0007).
Length and weight of the newborns and the gestational age did not differ between groups. Immediately after birth, rectal temperature of the newborns was near 37.5°C in all neonates (Fig. 3). No differences in rectal temperature between groups were detected immediately after birth, after 1 and 5 minutes, and at the beginning of the bonding period. Soon after the start of the bonding period, core temperature decreased in both groups; the core temperature of babies in the passive warming group was significantly lower than babies with active warming at 5, 10, 15 and 20 minutes of bonding (Fig. 3). At the end of the bonding period, mean (SD) rectal temperature of passively insulated babies was 35.9 (0.6)°C vs 37.0 (0.2)°C in actively warmed babies (P < 0.0001). Hypothermia was present in 17 of 21 (81%) of the passively warmed and in 1 of 19 (5%) of the actively warmed babies (P < 0.0001).
Mean skin temperature of the infants was not different 5 minutes after birth. However, at the end of the bonding period, it was significantly higher 35.2 (0.5)°C in actively warmed versus passively insulated infants (33.3 (1.3)°C) (Fig. 4).
Intermittent low-intensity shivering (grade 1) was present in 5 of 21 (24%) of the passively insulated and in none of the actively warmed parturients (P < 0.0001).
Both paired and unpaired analysis15,16 of the neonatal core temperatures from baseline to the end of the 20-minute bonding period were P < 0.0001.
The main finding of our study was that 81% of the newborns became hypothermic if they received standard passive warming during skin-to-skin bonding on the mother’s chest during cesarean delivery. Active cutaneous warming of the mothers, starting immediately after the establishment of the spinal block and continued during the bonding period, prevented hypothermia in 95% of the newborns. In addition, active warming increased mean skin temperature of the infants and their mothers’ core and skin temperatures. Thermal comfort was higher, and perioperative shivering was reduced in actively warmed mothers.
To our knowledge, this is the first clinical study demonstrating the rapid decrease of core temperature in newborns during bonding on the mother’s chest without any active warming. Without active cutaneous warming, mean maternal skin temperature was 2.4°C lower, and mean neonatal temperature approximately was 2°C lower than with active cutaneous warming. However, active warming as performed did not prevent a decrease of core temperature during bonding from 37.5 (0.2)°C to 37.0 (0.2)°C. Nevertheless, only one of 19 newborns became hypothermic, defined as a core temperature lower than 36.5°C.
Given our study design, we cannot clearly differentiate whether the forced-air warming blanket applied during bonding or “prewarming” of maternal skin resulting in higher skin temperatures before skin-to-skin contact mitigated infant heat loss. We hypothesize that both factors may play a role, but these mechanisms must be investigated in further studies.
In fact, neonates are at high risk for hypothermia,17 especially if they are premature, have low birth weight or a low Apgar score, or are delivered by cesarean delivery.8 Spontaneous labor, prolonged rupture of membranes, and antenatal steroid administration have been associated with decreased risk of hypothermia.8
After vaginal delivery, it is a common practice to place the newborn skin to skin on the mother’s chest. This “bonding position” of the newborn for the first 30 minutes of life is favored by most midwives to provide close interaction between mother and her child.11 Disruptions in maternal–infant bonding are correlated with pediatric bronchial asthma and were found to be related to physical separation at birth.18 Mothers who received extra contact exhibited significantly more affectionate behavior toward their infants than did the mothers who received routine care.19 As a result, midwives and mothers encourage bonding procedures not only after deliveries outside operating rooms but also during cesarean delivery in awake mothers under spinal or epidural anesthesia.
To our knowledge, no randomized trial has investigated the consequences of (mild) hypothermia in mature, healthy neonates. Although negative effects (i.e., acidosis, hypoxemia) seem likely in this population, effects on morbidity and mortality remain speculative. Nevertheless, prevention of hypothermia is considered one of the most essential elements of neonatal care. Forced-air warming systems with a ring-shaped cover as well as warming mattresses, plastic wraps, bags, or caps have been found to be efficient for maintaining body temperature.5,20
Mothers are also at risk of developing hypothermia during the procedure even when spinal21 or epidural anesthesia14 is performed. Intraoperative lower body forced-air warming alone does not prevent intraoperative hypothermia or shivering in women undergoing elective cesarean delivery with spinal anesthesia.21
Our study may be criticized because the temperature of the warm air was set to 44°C during the warming period that may have caused hyperthermia in the newborns. Lower temperatures, other neonatal warming devices, or warming either mother or newborn were not investigated but could be studied as topics of future research. However, our data showed that even this air temperature was not able to prevent a decrease in core temperature during bonding. Further, we measured rectal temperatures in the newborns and sublingual temperatures in the mothers that might differ from core temperatures. However, rectal temperature is close to core temperature, and the recommended method of temperature assessment in infants aged <2 years.22,23 In adult patients, sublingual temperature has been demonstrated to provide a high correlation with tympanic membrane temperature24 that reflects the temperature of the core thermal compartment.25
In our study, we planned a 20-minute bonding period for practical reasons because this is the average time period required to finish a cesarean delivery operation after clamping the umbilical cord. Longer bonding periods would not have been appropriate because at the end of surgery the mother–infant dyad is typically moved from the operating room to a recovery area. To our knowledge, there are no studies demonstrating any effect of shorter or longer bonding periods than 20 minutes.
Finally, we investigated healthy and stable newborns. Therefore, we cannot comment on the effects of forced-air skin-surface warming in preterm infants or very low birth weight or neonates with other conditions.
In summary, most newborns became hypothermic during a 20-minute bonding period on the mother’s chest during cesarean delivery in the operating room although they were covered with warm blankets. Hypothermia was prevented by active warming of the mothers and the babies with 44°C forced-air warming during the skin-to-skin bonding period.
Name: Jan Höcker, MD.
Contribution: This author helped design the study, analyze the data, and write the manuscript.
Attestation: Jan Höcker has seen the original study data, reviewed the analysis of the data, approved the final manuscript, and is the author responsible for archiving the study files.
Name: Berthold Bein, MD.
Contribution: This author helped design the study.
Attestation: Berthold Bein has seen the original study data, reviewed the analysis of the data, and approved the final manuscript.
Name: Ernst-Peter Horn, MD.
Contribution: This author helped design the study, analyze the data, and write the manuscript.
Attestation: Ernst-Peter Horn has seen the original study data, reviewed the analysis of the data, and approved the final manuscript.
Name: Kerstin Ramaker, MD.
Contribution: This author helped conduct the study.
Attestation: Kerstin Ramaker has seen the original study data, reviewed the analysis of the data, and approved the final manuscript.
Name: Markus Steinfath, MD.
Contribution: This author helped design the study.
Attestation: Markus Steinfath has seen the original study data and approved the final manuscript.
Name: Birgit Buchloh.
Contribution: This author helped conduct the study.
Attestation: Birgit Buchloh has seen the original study data and approved the final manuscript.
This manuscript was handled by: Cynthia A. Wong, MD.
We would like to thank Rita Kipf, R.N. and Ingeborg Meyer, R.N. for their assistance with the study.
1. Lunze K, Bloom DE, Jamison DT, Hamer DH. The global burden of neonatal hypothermia: systematic review of a major challenge for newborn survival. BMC Med. 2013;11:24
2. Christensson K, Siles C, Cabrera T, Belaustequi A, de la Fuente P, Lagercrantz H, Puyol P, Winberg J. Lower body temperatures in infants delivered by caesarean section than in vaginally delivered infants. Acta Paediatr. 1993;82:128–31
3. . Clinical-Practice-Guideline. The management of inadvertent perioperative hypothermia in adults. The National Collaborating Centre for Nursing and Supportive Care commissioned by National Institute for Health and Clinical Excellence (NICE): April 2008. Available at: http://guidance.nice.org.uk/CG65
4. Belsches TC, Tilly AE, Miller TR, Kambeyanda RH, Leadford A, Manasyan A, Chomba E, Ramani M, Ambalavanan N, Carlo WA. Randomized trial of plastic bags to prevent term neonatal hypothermia in a resource-poor setting. Pediatrics. 2013;132:e656–61
5. McCall EM, Alderdice F, Halliday HL, Jenkins JG, Vohra S. Interventions to prevent hypothermia at birth in preterm and/or low birthweight infants. Cochrane Database Syst Rev. 2010;1:CD004210
6. Leadford AE, Warren JB, Manasyan A, Chomba E, Salas AA, Schelonka R, Carlo WA. Plastic bags for prevention of hypothermia in preterm and low birth weight infants. Pediatrics. 2013;132:e128–34
7. Rong Z, Liu H, Xia S, Chang L. Risk and protective factors of intraventricular hemorrhage in preterm babies in Wuhan, China. Childs Nerv Syst. 2012;28:2077–84
8. Miller SS, Lee HC, Gould JB. Hypothermia in very low birth weight infants: distribution, risk factors and outcomes. J Perinatol. 2011;31(Suppl 1):S49–56
9. Chawla S, Amaram A, Gopal SP, Natarajan G. Safety and efficacy of Trans-warmer mattress for preterm neonates: results of a randomized controlled trial. J Perinatol. 2011;31:780–4
10. Kennell J, McGrath S. Starting the process of mother-infant bonding. Acta Paediatr. 2005;94:775–7
11. Dunn DM, White DG. Interactions of mothers with their newborns in the first half-hour of life. J Adv Nurs. 1981;6:271–5
12. Bauer K, Uhrig C, Sperling P, Pasel K, Wieland C, Versmold HT. Body temperatures and oxygen consumption during skin-to-skin (kangaroo) care in stable preterm infants weighing less than 1500 grams. J Pediatr. 1997;130:240–4
13. Ramanathan NL. A new weighting system for mean surface temperature of the human body. J Appl Physiol. 1964;19:531–3
14. Horn EP, Schroeder F, Gottschalk A, Sessler DI, Hiltmeyer N, Standl T, Schulte am Esch J. Active warming during cesarean delivery. Anesth Analg. 2002;94:409–14
15. Diehr P, Martin DC, Koepsell T, Cheadle A. Breaking the matches in a paired t-test for community interventions when the number of pairs is small. Stat Med. 1995;14:1491–504
16. Proschan MA. On the distribution of the unpaired t-statistic with paired data. Stat Med. 1996;15:1059–63
17. Macario A, Dexter F. What are the most important risk factors for a patient’s developing intraoperative hypothermia? Anesth Analg. 2002;94:215–20
18. Madrid A. Helping children with asthma by repairing maternal-infant bonding problems. Am J Clin Hypn. 2005;48:199–211
19. Anisfeld E, Lipper E. Early contact, social support, and mother-infant bonding. Pediatrics. 1983;72:79–83
20. Asaga T, Komatsu H, Chujo K, Ueki M, Yokono S, Ogli K. [Efficacy of ring-shape cover in active skin surface warming in neonates–a retrospective comparative study with conventional methods]. Masui. 1997;46:1362–7
21. Butwick AJ, Lipman SS, Carvalho B. Intraoperative forced air-warming during cesarean delivery under spinal anesthesia does not prevent maternal hypothermia. Anesth Analg. 2007;105:1413–9
22. Batra P, Saha A, Faridi MM. Thermometry in children. J Emerg Trauma Shock. 2012;5:246–9
23. Robinson JL, Seal RF, Spady DW, Joffres MR. Comparison of esophageal, rectal, axillary, bladder, tympanic, and pulmonary artery temperatures in children. J Pediatr. 1998;133:553–6
24. Höcker J, Bein B, Böhm R, Steinfath M, Scholz J, Horn EP. Correlation, accuracy, precision and practicability of perioperative measurement of sublingual temperature in comparison with tympanic membrane temperature in awake and anaesthetised patients. Eur J Anaesthesiol. 2012;29:70–4
25. Sessler DI. Temperature monitoring and perioperative thermoregulation. Anesthesiology. 2008;109:318–38