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Newborn skin temperature two days postpartum during breastfeeding related to different labour ward practices
Early Human Development (2007) 83, 55 — 62
available at www.sciencedirect.com
www.elsevier.com/locate/earlhumdev
Newborn skin temperature two days postpartum during breastfeeding related to different labour ward practices W. Jonas a,*, I. Wiklund b, E. Nissen a,c, A.-B. Ransjo ¨-Arvidson a, K. Uvna ¨s-Moberg d a
Department of Women and Child Health, Division for Reproductive and Perinatal Health Care, Karolinska Institute, Retzius Va ¨g 13a, 17177 Stockholm, Sweden b KIDS Division of Obstetrics and Gynecology, Karolinska Institute, Danderyds Hospital, 18288 Stockholm, Sweden c School of Life Sciences, University of Sko ¨vde, Box 408, 541 28 Sko ¨vde, Sweden d Department of Animal Environment and Health, Swedish University of Agriculture, Box 234, 532 23 Skara, Sweden Accepted 25 April 2006
KEYWORDS Breastfeeding; EDA; Oxytocin; Skin-to-skin contact; Temperature
Abstract Aim: To investigate (1) the skin temperature pattern in newborns two days after birth in connection to breastfeeding and to examine (2) if the administration of epidural analgesia (EDA) and oxytocin (OT) infusion during labour influences this parameter at this point of time. Method: Forty-seven mother—infant pairs were included in the study: nine mothers had received OT stimulation during labour (OT group), 20 mothers had received an EDA and OT during labour (EDA group), while 18 mothers had received neither EDA nor OTstimulation during labour (control group). A skin temperature electrode was attached between the newborn’s shoulder blades. The newborn was placed skin-to-skin on the mother’s chest and covered with a blanket. The temperature was recorded immediately after the newborn was put on the mother’s chest and at 5, 10, 20 and 30 min. Results: The temperature measured when the newborns were put skin-to-skin on their mothers’ chest was significantly higher in the infants of the EDA group (35.07 8C) when compared to the control group (34.19 8C, p = 0.025). Skin temperature increased significantly ( p = 0.001) during the entire experimental period in the infants belonging to the control group. The same response was observed in infants whose mothers received OT intravenously during labour ( p = 0.008). No such rise was observed in infants whose mothers were given an EDA during labour. Conclusion: The results show that the skin temperature in newborns rises when newborns are put skin-to-skin to breastfeed two days postpartum. This effect on temperature may be hampered by medical interventions during labour such as EDA. D 2006 Elsevier Ireland Ltd. All rights reserved.
* Corresponding author. Tel.: +46 8 52482410; fax: +46 8 52482400. E-mail address: [email protected] (W. Jonas). 0378-3782/$ - see front matter D 2006 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.earlhumdev.2006.05.001
56
1. Introduction A normal physiologic response directly following birth is that the temperature of the newborn rises. If the newborn is immediately placed in a skin-to-skin position with the mother the temperature exhibits a more pronounced rise. The mechanism behind this is not known [1]. It is likely that maternal transfer of warmth to the baby plays an important role — in particular since the mother’s breast temperature also increases in response to skin-to-skin contact and breastfeeding [2]. During skin-to-skin contact maternal oxytocin levels rise and there is even a relationship between the intensity of the baby’s hand movements and oxytocin levels [3,4]. The rise of maternal temperature may activate sensory nerves in the infant. Such stimulation induces calm and relaxation by decreasing the sympathetic tone in the infant. One consequence of this is vasodilatation in the skin, which results in higher skin temperature. In a recent study by Bystrova et al. [1] the newborns’ skin temperature was measured in the axilla, interscapularly, and on the thigh and foot in response to skin-to-skin contact. It was found that the rise in skin temperature was especially pronounced in the feet. That supports the assumption that enhanced cutaneous vasodilatation plays an important role in the regulation of skin temperature. Whether the infant’s skin temperature rises also in response to skin-to-skin contact and breastfeeding later on during the perinatal period is not known. During the last decades in Sweden routines regarding normal childbirth have changed. The administration of epidural analgesia (EDA) has become a common intervention and in 2002, 39% of all primiparae received EDA at the clinic where the present study was conducted. Another common intervention at this clinic is to administer oxytocin (OT) infusion in order to augment labour. Fifty percent of all primiparaes who gave birth received this type of intervention [5]. Since these interventions have become widely accepted, there is an increasingly important need to investigate whether these interventions influence the physiology of the mother and infant immediately following birth and/or in the long-term. It has previously been demonstrated that EDA administration during labour may influence the temperature of the mother and her newborn. A rise (0.14 8C per hour) in maternal temperature was observed within the first hours following EDA treatment [6], and maternal fever was also observed during labour after EDA administration [7,8]. Other studies report an increase in the temperature of the fetus following in utero exposure to EDA [9]. A previous study performed by our group showed that the skin temperature of newborns whose mothers had been exposed to EDA and other kinds of pain relief was further elevated 45 min postpartum when compared to nonexposed infants [10]. Also, OT administration during labour has been shown to be followed by an increased fetal temperature [11]. There are no studies that have scrutinized the effects of EDA or OT administration during labour on the temperature of the newborn in connection with skin-to-skin contact and breastfeeding later on in the perinatal period. The aim of this study was twofold: to investigate (1) the skin temperature pattern in newborns two days after birth in
W. Jonas et al. connection to breastfeeding and to examine (2) if EDA administration and OT infusion during labour influence this parameter at this point in time.
2. Participants and methods 2.1. Study sample The study was conducted at one of the six maternity hospitals in Stockholm, Sweden. The mother—infant pairs were consecutively recruited on Mondays to Fridays during research weeks from January 2002 to December 2003. The hospital at which the study took place is located in an area with high educational level and good socio-economic status. However, the maternity routines do not differ from hospitals in the rest of Sweden. The following inclusion criteria had to be fulfilled: The mothers had to be Swedish speaking primiparae with an uncomplicated singleton pregnancy and a normal labour. The newborns had to be born at full term with an Apgar score of 8 or more at 1 min postpartum. The mother and her infant should not have been separated after birth not even for medical examinations. The newborns should have been exclusively breastfed and not been given any formula. The experiment was performed two days after birth. The mothers met the researchers about 10 to 24 h after delivery, when the research team (WJ or IW) informed the mothers about the ongoing study. The mothers were told that the researchers wanted to study some physiological and psychological parameters related to breastfeeding at 24—48 h after birth in mothers and infants. If the mother gave her written informed consent she was instructed to call for the researchers the next morning when the newborn showed signs of wanting to breastfeed (e. g. rooting, tongue movements). The mother—infant pairs were allocated to three groups depending on the treatments the mothers had received during and after labour: mothers who had received OT stimulation during labour (OT group, n = 9), mothers who had been exposed to EDA and OT infusion during labour (EDA group, n = 20), and mothers who had received neither EDA nor OT stimulation during labour (control group, n = 18). In total, 47 mother—infant pairs were included in the study. Fourteen mothers declined from participation. Of those, two mothers had received OT infusion during labour, 10 mothers had an EDA and OT infusion during labour and two mothers had no intervention at all.
2.2. Maternity routines after birth According to standard maternity routines, all healthy newborns are placed skin-to-skin with their mothers immediately after birth. The newborns remain on their mothers’ chests until the first breastfeeding is established or until the newborns fall asleep. Usually the partners of the women are present during and after childbirth. Rooming-in is practised. The maternity rooms are designed to facilitate an bat-home-feelingQ and to allow parents to interact with their newborn.
Infant temperature and breastfeeding
2.3. Experimental design All breastfeeding observations took place in the morning and were always conducted by the same two research midwives (WJ and IW). Before the experiment started, all newborns were lying with their clothes on in the bed of their mothers. The newborns were then undressed and were weighed having a diaper on. Thereafter a skin temperature electrode (Ellab, Copenhagen, Denmark; accuracy +/ 0.1 8C) was attached between the shoulder blades. Interscapular temperature measurements were chosen for practical reasons, in that placing an electrode between the shoulder blades was not only technically easier, it also avoided disturbing the breastfeeding behaviour of the infant. The newborns were then immediately placed skin-to-skin on the mothers’ chest and were covered with a light blanket in order to maintain body temperature. This procedure took 3 min. The first temperature recording was performed as soon as skin-toskin contact with the mother was established. Following this, interscapular temperature readings were performed at 5, 10, 20, and 30 min after skin-to-skin contact was established. The time of the onset as well as the duration of suckling was registered. If the breastfeeding finished before 30 min had passed, the mothers kept the newborns in their arms irrespective of breastfeeding. For the purposes of this study, the environmental temperature in the maternity rooms was monitored and found to vary between 22 and 24.4 8C.
2.4. Ethical considerations The study was approved by the Ethics committee, Karolinska Institute, Stockholm.
3. Statistical analysis For the statistical analysis of the data, the SPSS program (Statistical Package for the Social Sciences) version 12.0 was used [12]. The median (md) and interquartile distances Table 1
57 (Q25—Q75) were used to describe background variables and outcome data that were non-parametrically distributed. Temperature measurements are presented as means (m), standard errors of the mean (SE), and range (R). The mean values of temperature recorded at 10, 20 and 30 min were calculated. For testing temperature differences between the groups unpaired t-tests were used and to test the differences within the groups over time paired t-tests were used. To correlate newborn age to temperature the Pearson’s correlation coefficient was calculated. In order to test differences between the groups regarding background variables, the Mann—Whitney U-test for independent samples and the v 2 test were used for interval and category data, respectively. An exploratory multiple regression analysis was performed to study the impact of different background variables on the temperature differences in the first ten minutes of the observation period. Since the temperature recordings were only recorded every five minutes in the beginning of the study period, it is not possible to disentangle the effects on temperature of skin-to-skin contact and onset of suckling. In order to elucidate whether the temperature rise was due to skin-toskin contact or breastfeeding, the obtained temperature values were regrouped according to the onset of suckling. Some newborns started to suckle the breast within the first four minutes of the observation period. Thus, for those newborns the temperature obtained at skin-to-skin contact was also the temperature considered before the onset of suckling. In the newborns who started to breastfeed between five and nine minutes of the observation period, the temperature obtained at 5 min was considered as the temperature before suckling. For the newborns who started to suckle the breast between 10 and 20 min, the temperature recorded at 10 min was counted as the temperature before the onset of suckling. Those obtained temperature readings were then summarized and thus, a new variable bTemperature before the onset of sucklingQ was created. The first measurement of temperature following the onset of suckling in each individual was called bTemperature after the onset of suckling 1Q and the
Clinical characteristics of mothers and their newborns (median, Q25—Q75 and frequencies)
Maternal age (yrs) 1st stage of labour (h) 2nd stage of labour (min) Blood loss (ml) OT infusion before birth (h) Oxytocin before birth (ml) Oxytocin after birth (ml) Duration of EDA (h) Marcain (mg) Sufenta (Ag) Use of N2O (yes) Acupuncture (yes) Number of boys/girls Weight (g)
Control group (n = 18)
Oxytocin group (n = 9)
EDA group (n = 20)
p-value+
31 (27—33) 7.0 (4.5—9.4) 38 (28—60) 367.50 (260—500)
32 (28—33) 9.1 (8.4—11.0) 63 (43—70) 375 (237—850) 1 (0:50—4) 81.5 (32.25—164.75) 154.5 (23.25—450.75)
ns ns ns ns c) ns c) ns c) ns
10 5 8/10 3450 (3163—3751)
9 2 5/4 4030 (3252—4195)
31 (29—33) 11.1 (7.2—12.1) 35 (22—51) 490 (262—637) 1:45 (0:45—4:83) 95.5 (43—199) 340 (125—433.5) 3:37 (2:24—5:37) 22.5 (17.5—42.5) 12.5 (10—35) 17 6 11/9 3423 (3345—3725)
+ Comparisons (Mann—Whitney or v 2 test) were made between the a) control- and OT group, and b) control- and EDA group. If variables were empty in the control group, comparisons were made between the c) OT- and EDA group.
b) 0.05 ns ns a) 0.059
58
W. Jonas et al.
Table 2
Breastfeeding characteristics (median, Q25—Q75) at time of experiment
Neonatal age (h) Number of breastfeedings after birth Minutes from skin-to-skin contact to onset of suckling Breastfeeding duration (min) a
Control group (n = 18)
Oxytocin group (n = 9)
EDA group (n = 20)
p-valuea
36 (25—39) 7.5 (5—10.25)
36 (35—45) 6 (5—11)
33 (27—40) 6 (4.2—8.7)
ns ns
2 (1—9)
3 (0—12)
2 (1—5)
ns
30 (21—37)
22 (16—39)
21 (15—31)
ns
The Mann—Whitney test was computed between the control group and the study groups.
measurement obtained when all newborns had suckled the breast for five minutes or longer was called bTemperature after the onset of suckling 2Q.
4.4. Temperature pattern during skin-to-skin contact and breastfeeding
4. Results
During the first ten minutes of observation the temperature rose significantly in the control group (+ 0.91 8C, p = 0.001). The temperature remained at a plateau level (35 8C) during the rest of the observation period. A rise in temperature was also observed in the OT group in which the temperature increased by 1.47 8C ( p = 0.008) and remained stable around 36 8C. The EDA group showed a significant temperature decrease of 0.62 8C ( p = 0.019) during the first ten minutes, before remaining relatively stable (Table 3b; Fig. 1). When the mean values of the temperature recordings obtained at 10, 20 and 30 min were compared between the different groups the levels in the OT group were significantly higher than those of the control group ( p = 0.048). In contrast, the temperature of the EDA group did not differ from the control group (Table 3a).
4.1. Background data The obstetrical background data were collected from the maternity records. The clinical characteristics of mothers and their newborns and the outcome data of the breastfeed are documented in Tables 1 and 2. The only statistically significant difference between the groups was found regarding the use of N2O. The number of mothers who received N2O was greater in the EDA group compared with mothers of the control group ( p = 0.05). None of the mothers were smokers, and 75% of the mothers had a university degree.
4.2. State of the infants
4.5. Temperature in relation to the onset of suckling
All newborns were awake and hungry but calm before they started to suckle. None of the newborns cried.
4.3. Temperature at skin-to-skin contact When temperature recordings commenced the interscapular temperature of the newborns belonging to the control group was 34.19 C8. The temperature was initially slightly higher in the OT group (34,42 8C) than in the controls and the EDA group had the highest temperature (35,07 8C). The temperature in the EDA group was significantly higher than the temperature obtained in the control group ( p = 0.025) (Table 3a; Fig. 1). In the EDA group, the age of the newborn was negatively correlated to the mean temperature, indicating that the younger the infant the higher the temperature when the experiment started (r = 0.46, p = 0.04). Table 3a
For assessing the effect of suckling on temperature, the difference between the bTemperature before the onset of sucklingQ and bTemperature after the onset of suckling 1Q was calculated. The temperature rose significantly following the start of suckling in the control group (0.78 8C, p = 0.003), and also in the OT group (0.90 8C, p = 0.06). The temperature in the EDA group, however, did not increase significantly after onset of suckling (Table 3b; Fig. 2). Interestingly, the temperature in the newborns of the OT group started to rise immediately at skin-to-skin contact and not, as in the control group, after the onset of suckling. This suggests that an effect on temperature had occurred already as a response to skin-to-skin contact between mother and the newborn (Fig. 2). When the values bTemperature before the onset of sucklingQ and bTemperature after the onset of suckling 2Q
Newborn temperature data presented as mean, standard errors (SE) and range (R)
Differences in temperature between the following measurement Initial temperature Mean temperature (10—30 min)
Control group (CG) (n = 18)
Oxytocin group (OTG) (n = 9)
EDA group (EDA) (n = 20)
p-value
Mean
SE
R
Mean
SE
R
Mean
SE
R
CG/OTG
CG/EDA
34.19 34.94
0.26 0.28
3.5 3.70
34.42 35.86
0.3 0.34
1.90 2.92
35.07 34.69
0.26 0.29
3.30 4.13
ns 0.048
0.025 ns
P-values refer to differences between groups.
Infant temperature and breastfeeding
59
Figure 1 The interscapular temperature pattern (m, bars showing the standard error of the mean (SE)) of healthy newborns in the oxytocin (-E-), EDA group (-n-) and the control (-o-) during the first 30 min of a breastfeed day two postpartum. At b0Q skin-to-skin contact was established. A different temperature pattern was found in the three groups.
Figure 2 The interscapular temperature pattern of the oxytocin- (-E-), EDA- (-n-), and control- (-o-) groups when temperature values (m, bars presenting the standard error of the mean (SE)) were organized regarding the onset of suckling. A detailed explanation is given in the Statistics section.
were compared, the temperature in the control group continued to rise (0.96 8C, p = 0.001), but not in the other two groups (Table 3b). This suggests that the suckling stimulus has the function of a bsecond triggerQ on the temperature rise.
The only variable that showed a significant impact on the temperature difference was having an EDA ( p V 0.001). Altogether, these variables explained 64.6% of the variation in the temperature differences observed in connection to the onset of suckling ( p = 0.001).
4.6. Regression analysis To investigate the influence of other variables a multiple exploratory regression analysis was performed (Table 4). The dependent variable was bTemperature difference between skin-to-skin contact and temperature value at 10 minQ. The independent variables were 1) Oxytocin (0/1), 2) EDA (0/1), 3) oxytocin infusion before birth (ml), 4) duration of 2nd stage of labour (min), 5) acupuncture (0/ 1), 6) N2O (0/1), 7) neonatal age (h) at experiment, 8) number of breastfeedings after birth, and 9) neonatal weight (g) at birth.
Table 3b
5. Discussion The main findings in the present study were that breastfeeding two days after birth results in a rise in the interscapular temperature in infants and that the expression of this rise is dependent on whether or not the mothers received EDA and/or OT infusion during labour. One of the limitations of the study is that only interscapular temperature measurements were obtained.
Newborn temperature data presented as mean differences, standard error of the mean (SE) and range (R)
Temperature at skin-to-skin contact — temperature at 10 min Temperature before the onset of suckling — temperature after the onset of suckling 1 Temperature before the onset of suckling — temperature after the onset of suckling 2
Control group (CG) (n = 18)
Oxytocin group (OTG) (n = 9)
EDA group (n = 20)
Mean diff
SE
R
Mean diff
SE
R
Mean diff
0.91
0.2
3.1
1.47
0.37
2.7
0.78
0.20
2.8
0.90
0.38
0.96
0.21
3.1
0.70
0.45
p-value
SE
R
CG
OTG
EDA
0.62
0.22
2.4
0.001
0.008
0.019
2.7
0.18
0.19
2.4
0.003
0.06
ns
3.1
0.33
0.23
2.3
0.001
ns
ns
P-values refer to differences over time within each group as calculated below.
60 Table 4
W. Jonas et al. Regression analysis
Model
B-coefficient
SE
Constant Oxytocin (0/1) EDA (0/1) Acupuncture (0/1) Use of N2O (0/1) OT before birth (ml) Duration 2nd stage of labour (min) Neonatal weight (g) Neonatal age (h) Number of breastfeedings since birth
0.795 0.360 1.697 0.538 0.673 0.081 0.000 2.334E 05 0.019 0.067
1.569 0.574 0.408 0.363 0.376 0.151 0.000 0.000 0.025 0.062
t-value 0.507 0.628 4.160 1.482 1.789 0.091 0.138 0.009 0.125 0.177
p-value 0.617 0.536 0.000 0.151 0.086 0.598 0.343 0.946 0.448 0.294
Dependent variable: temperature difference between the temperature at 10 min and skin-to-skin contact (df = 9, R 2 = 64.6%, Adjusted R 2 = 51.9%, overall significance p = 0.001).
However, in earlier studies conducted by our group the interscapular temperature of the newborn was measured [1,10,13]. Those studies showed that the interscapular temperature values correlated well with temperature measurements obtained at other parts of the body, i.e. the axilla, thigh and foot. Another limitation of the study is that randomization of mothers before birth to either OT infusion or EDA treatment is impossible for practical and ethical reasons. However, our participants were consecutively selected following strict inclusion criteria. The participants were derived from a very homogenous group of women suggesting that the material is representative for the use of the interventions at the clinic where the study was performed. It is well known that infants’ temperature naturally increases postpartum [10,13]. If the baby is placed in skinto-skin contact with the mother the temperature exhibits a further rise [1]. Our novel finding of a rise of newborns’ skin temperature during breastfeeding and skin-to-skin contact two days after birth suggests that the infant responds in a similar way at this point in time as when being placed skin-to-skin immediately postpartum. After birth the infant is exposed to lower environmental temperatures and sympathetic fibers innervating the brown fat tissue are activated and heat is generated through lipolytic processes [14]. It is also known that heat production increases after ingestion of a meal in infants [14]. Whether skin-to-skin contact and suckling trigger also heat production by increasing lipolytic processes is not known, but remains a possibility [14]. However, the degree of vasodilatation in cutaneous blood vessels is of importance for the temperature recorded in the skin. Therefore, variations in the balance between cutaneous vasoconstriction and vasodilatation will also be of importance for the temperature levels obtained [2,15]. In a recent study we were able to show that the rise of infants’ skin temperature postpartum was dependent on maternity routines. The foot temperature for example exhibited a clear rise in response to skin-to-skin treatment and a fall after separation from the mother [1]. The exaggerated rise of foot temperature in the skin-to-skin group suggests that part of the increase in temperature is due to a change in the autonomic nervous tone resulting in reduced sympathetic nerve activity and consequent cutaneous vasodilatation.
The stress of being born is accompanied by an increased activity in the sympathetic nervous system, peripheral vasoconstriction and a reduction in skin temperature [16]. In contrast, touch and warmth, as during skin-to-skin contact activate cutaneous sensory nerves which lead to a reduction of the sympathetic nervous tone [17]. Consequently, peripheral circulation is enhanced, which is followed by an increased skin temperature in e.g., the foot [1]. Touch and warmth applied on the chest are particularly powerful stimuli to antagonize stress, due to the presence of a particular kind of afferent nerves originating from this area [18]. In addition to the sensory fibers innervating the spinal cord, these signals reach the CNS via the ganglion nodosum and the nucleus tractus solitarius (NTS) [15,18]. There is a direct connection between the NTS and the oxytocinergic nerves in the paraventricular nucleus (PVN). The oxytocinergic nerves emanating from the PVN subsequently reach many regulatory areas in the brain. OT exerts inhibitory effects on sympathetic nervous tone and the release of OT may therefore contribute to the antistress effect exerted by bnon-noxiousQ sensory stimulation of the skin, in particular if triggered from the ventral side of the chest. OT has been shown to be released both into the circulation and into the CNS in response to warmth and touch in a rat model [19]. No such direct observations have been done in humans. However, suggestive evidence for the release of OT in the CNS is provided by two studies showing a relationship between personality changes and the levels of OT in connection with breastfeeding [20,21]. In addition to skin-to-skin contact, suckling also induces activation of vagal nerve afferents, which may be followed by an enhanced vagal tone and antistress effects of the type described above as induced by skin-to-skin contact [22]. Therefore, the rise of infants’ interscapular skin temperature during breastfeeding two days after birth may be related to suckling, as well as to skin-toskin contact. However, our data showing that the rise of temperature had started before the onset of suckling in the OT group suggests that the skin-to-skin contact was an important factor in triggering these responses. Unfortunately, due to the design of the study, it is not possible to disentangle the effects caused by skin-to-skin contact per se and suckling. The medical interventions applied to the mother during labour influenced the temperature response. In those
Infant temperature and breastfeeding infants whose mothers had received an OT infusion during labour, the response was exaggerated. Possibly OT is responsible for these effects. In order to induce these effects OT has to reach the CNS of the infant. Malek et al. [23] scrutinized both the maternal—fetal and the fetal—maternal placental diffusion of OT in vitro and found that more OT is transferred to the fetus than back to the mother. Thus, OT infusion given during labour could reach the circulation of the fetus and may thus induce the effects in response to OT infusion as observed in the present study. A limited percentage of exogenous OT passes the blood— brain barrier of adult animals [24,25]. However, since the blood—brain barrier is not fully developed in the neonatal period under consideration larger amounts may enter the CNS at this age. This opens up for the possibility that maternal OT infusion during labour may reach the brain of the fetus to induce effects observed in the present study. Results from animal experiments show that repeated exposure to OT in the postnatal period gives rise to lifelong effects. These effects include antistress-like effects, such as the lowering of blood pressure [26] and corticosterone levels [22], an increased pain threshold and weight gain [27]. The effects are sometimes not apparent until adulthood [28,29]. The effects of skin temperature in the infant observed in the present study may be a consequence of an altered autonomic nervous balance. A higher parasympathetic nervous tone may be related to increased circulation in the skin and hence a higher temperature. In those infants whose mothers received EDA during labour the initial temperature was higher and the consequent rise of temperature during breastfeeding was abolished. EDA is known to enhance the temperature in mothers during labour and in both mothers and infants after birth [6— 9]. The effects have been suggested to be a consequence of an influence on the center of temperature regulation both in mothers and infants [30]. The reasons for this are unknown. The higher initial temperature recorded in infants having been exposed to EDA in the present study may reflect a remaining effect of an early disturbance of the temperature regulation. This assumption is supported by the fact that the initial temperature obtained in infants of the EDA group was inversely related to age of these infants; in other words, the higher the temperature, the younger the infant. The second finding that infants from the EDA group did not display a rise of temperature in response to breastfeeding is more difficult to explain. Hypothetically, the effect might be due to decreased levels of OT in the brain of the infant. EDA is known to decrease OT levels during labour but the mechanism behind this effect is not fully understood. One possibility is that the EDA, when blocking the activity from the afferent nerves from the uterus, not only blocks the transmission in nerve fibers mediating pain but also those mediating OT release into the maternal circulation and brain which might lead to a reduction of OT levels. Another possibility that must be considered is that the opioid component of the EDA inhibits OT release. Opioids are known to inhibit the release of OT [31]. Sufentanil, which was used in the present study, may leak out into the maternal circulation and decrease OT release. The brain of the infant may however also be influenced directly by
61 sufentanil, since this substance is highly fat-soluble and has been shown to cross the placental barrier by passive diffusion, to accumulate in placental tissue, and to reach the circulation of the infant [32]. It also quickly penetrates the blood—brain barrier. Even though levels of sufentanil are very low in the umbilical blood vessels it is likely that they could still influence the newborns’ brain [33]. If so, not only maternal OT release but also that of the infant may be inhibited during and after birth, as long as the active metabolites are still present in the circulation. Assuming that the EDA by various mechanisms reduces the infant’s OT levels during a very critical period of life, the attunement of the autonomous nervous tone normally occurring at this point of time might be influenced. The lack of a temperature change during breastfeeding two days after birth might be an expression of this. An intriguing and compelling question is whether relative reduction in OT exposure during the perinatal period not only produces changes in thermoregulation some time after birth but may also influence cardiovascular function and pain. It is important to notice that the above-mentioned results are preliminary and that the explanations still remain speculative. Further studies are needed to corroborate the findings since the effects observed for the labour ward interventions on the skin temperature of the newborn may be due to completely different, and as yet unknown, factors. However, if the effects described above are, in fact, consequences of labour ward routines, it is of immense importance to demonstrate and describe them in detail since the manifestations of these effects in particular may become more pronounced in adulthood. Given the large numbers of women receiving these treatments, even minor effects on newborns might have important future physiological and behavioural consequences for the human population.
Acknowledgments The authors would like to thank all mothers and newborns participating in this study and the staff at BB-Stockholm. Also, we would like to thank the Va ˚rdal Stiftelsen, the Swedish Research Council (K 1999-2001 27P-13085 and K 1999-27XP-13263-01), the Centre for Health Care Sciences at the Karolinska Institute and Praktikertja ¨ nst AB for research grants.
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W. Jonas et al. caesarean section or by the vaginal route. Early Hum Dev 1996;45:103 – 18. Statistics from BB Stockholm Maternity Ward; available from http://www.bbstockholm/se/stat_3html; 2003. Fusi L, Steer PJ, Maresh MJ, Beard RW. Maternal pyrexia associated with the use of epidural analgesia in labour. Lancet 1989;1:1250 – 2. Philip J, Alexander JM, Sharma SK, Leveno KJ, McIntire DD, Wiley J. Epidural analgesia during labor and maternal fever. Anesthesiology 1999;90:1271 – 725. Vinson DC, Thomas R, Kiser T. Association between epidural analgesia during labor and fever. J Fam Pract 1993; 36:617 – 22. Macaulay JH, Bond K, Steer PJ. Epidural analgesia in labor and fetal hyperthermia. Obstet Gynecol 1992;80:665 – 9. Ransjo ¨-Arvidson AB, Matthiesen AS, Lilja G, Nissen E, Widstro ¨m AM, Uvna ¨s-Moberg K. Maternal analgesia during labor disturbs newborn behavior: effects on breastfeeding, temperature, and crying. Birth 2001;28:5 – 12. Beck LR, Flowers CE Jr, Blair WD. The effects of oxytocin on fetal scalp temperature. Obstet Gynecol 1979;53:200 – 2. SPSS — Statistical Package for the Social Sciences, version 12.0. In. Chicago; 2004. Christensson K, Siles C, Moreno L, Belaustequi A, De La Fuente P, Lagercrantz H, et al. Temperature, metabolic adaptation and crying in healthy full-term newborns cared for skin-to-skin or in a cot. Acta Paediatr 1992;81:488 – 93. Mc Intire JHD, Nedergaard J, Cannon B. Thermoregulation. In: Gluckman PD, editor. Pediatrics and perinatology. London7 Arnold; 1996. p. 579 – 89. Eriksson M, Lundeberg T, Uvna ¨s-Moberg K. Studies on cutaneous blood flow in the mammary gland of lactating rats. Acta Physiol Scand 1996;158:1 – 6. Hagnevik K, Faxelius G, Irestedt L, Lagercrantz H, Lundell B, Persson B. Catecholamine surge and metabolic adaptation in the newborn after vaginal delivery and caesarean section. Acta Paediatr Scand 1984;73:602 – 9. Olausson H, Lamarre Y, Backlund H, Morin C, Wallin BG, Starck G, et al. Unmyelinated tactile afferents signal touch and project to insular cortex. Nat Neurosci 2002;5:900 – 4. Eriksson M, Lindh B, Uvna ¨s-Moberg K, Ho ¨kfelt T. Distribution and origin of peptide-containing nerve fibres in the rat and human mammary gland. Neuroscience 1996;70:227 – 45. Uvna ¨s-Moberg K, Bruzelius G, Alster P, Lundeberg T. The antinociceptive effect of non-noxious sensory stimulation is mediated partly through oxytocinergic mechanisms. Acta Physiol Scand 1993;149:199 – 204.
[20] Nissen E, Gustavsson P, Widstro ¨m AM, Uvna ¨s-Moberg K. Oxytocin, prolactin, milk production and their relationship with personality traits in women after vaginal delivery or cesarean section. J Psychosom Obstet Gynaecol 1998;19: 49 – 58. [21] Uvna ¨s-Moberg K, Widstro ¨m AM, Nissen E, Bjo ¨rvell H. Personality traits in women 4 days post partum and their correlation with plasma levels of oxytocin and prolactin. J Obstet Gynecol 1990;11:261 – 73. [22] Petersson M, Hulting AL, Uvna ¨s-Moberg K. Oxytocin causes a sustained decrease in plasma levels of corticosterone in rats. Neurosci Lett 1999;264:41 – 4. [23] Malek A, Blann E, Mattison DR. Human placental transport of oxytocin. J Matern Fetal Med 1996;5:245 – 55. [24] Richard P, Moos F, Freund-Mercier MJ. Central effects of oxytocin. Physiol Rev 1991;71:331 – 70. [25] Uvna ¨s-Moberg K, Petersson M. Oxytocin, a mediator of antistress, well-being, social interaction, growth and healing. Z Psychosom Med Psychother 2005;51:57 – 80. [26] Petersson M, Alster P, Lundeberg T, Uvna ¨s-Moberg K. Oxytocin causes a long-term decrease of blood pressure in female and male rats. Physiol Behav 1996;60:1311 – 5. [27] Uvna ¨s-Moberg K, Alster P, Petersson M, Sohlstrom A, Bjo ¨rkstrand E. Postnatal oxytocin injections cause sustained weight gain and increased nociceptive thresholds in male and female rats. Pediatr Res 1998;43:344 – 8. [28] Diaz-Cabiale Z, Olausson H, Sohlstrom A, Agnati LF, Narvaez JA, Uvna ¨s-Moberg K, et al. Long-term modulation by postnatal oxytocin of the alpha 2-adrenoceptor agonist binding sites in central autonomic regions and the role of prenatal stress. J Neuroendocrinol 2004;16:183 – 90. [29] Sohlstrom A, Carlsson C, Uvna ¨s-Moberg K. Effects of oxytocin treatment in early life on body weight and corticosterone in adult offspring from ad libitum-fed and food-restricted rats. Biol Neonate 2000;78:33 – 40. [30] Mercier FJ, Benhamou D. Hyperthermia related to epidural analgesia during labor. Int J Obstet Anesth 1997;6:19 – 24. [31] Rahm VA, Hallgren A, Ho ¨gberg H, Hurtig I, Odlind V. Plasma oxytocin levels in women during labor with or without epidural analgesia: a prospective study. Acta Obstet Gynecol Scand 2002;81:1033 – 9. [32] Krishna BR, Zakowski MI, Grant GJ. Sufentanil transfer in the human placenta during in vitro perfusion. Can J Anaesth 1997;44:996 – 1001. [33] Loftus JR, Hill H, Cohen SE. Placental transfer and neonatal effects of epidural sufentanil and fentanyl administered with bupivacaine during labor. Anesthesiology 1995;83:300 – 8.
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Newborn skin temperature two days postpartum during breastfeeding related to different labour ward practices W. Jonas a,*, I. Wiklund b, E. Nissen a,c, A.-B. Ransjo ¨-Arvidson a, K. Uvna ¨s-Moberg d a
Department of Women and Child Health, Division for Reproductive and Perinatal Health Care, Karolinska Institute, Retzius Va ¨g 13a, 17177 Stockholm, Sweden b KIDS Division of Obstetrics and Gynecology, Karolinska Institute, Danderyds Hospital, 18288 Stockholm, Sweden c School of Life Sciences, University of Sko ¨vde, Box 408, 541 28 Sko ¨vde, Sweden d Department of Animal Environment and Health, Swedish University of Agriculture, Box 234, 532 23 Skara, Sweden Accepted 25 April 2006
KEYWORDS Breastfeeding; EDA; Oxytocin; Skin-to-skin contact; Temperature
Abstract Aim: To investigate (1) the skin temperature pattern in newborns two days after birth in connection to breastfeeding and to examine (2) if the administration of epidural analgesia (EDA) and oxytocin (OT) infusion during labour influences this parameter at this point of time. Method: Forty-seven mother—infant pairs were included in the study: nine mothers had received OT stimulation during labour (OT group), 20 mothers had received an EDA and OT during labour (EDA group), while 18 mothers had received neither EDA nor OTstimulation during labour (control group). A skin temperature electrode was attached between the newborn’s shoulder blades. The newborn was placed skin-to-skin on the mother’s chest and covered with a blanket. The temperature was recorded immediately after the newborn was put on the mother’s chest and at 5, 10, 20 and 30 min. Results: The temperature measured when the newborns were put skin-to-skin on their mothers’ chest was significantly higher in the infants of the EDA group (35.07 8C) when compared to the control group (34.19 8C, p = 0.025). Skin temperature increased significantly ( p = 0.001) during the entire experimental period in the infants belonging to the control group. The same response was observed in infants whose mothers received OT intravenously during labour ( p = 0.008). No such rise was observed in infants whose mothers were given an EDA during labour. Conclusion: The results show that the skin temperature in newborns rises when newborns are put skin-to-skin to breastfeed two days postpartum. This effect on temperature may be hampered by medical interventions during labour such as EDA. D 2006 Elsevier Ireland Ltd. All rights reserved.
* Corresponding author. Tel.: +46 8 52482410; fax: +46 8 52482400. E-mail address: [email protected] (W. Jonas). 0378-3782/$ - see front matter D 2006 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.earlhumdev.2006.05.001
56
1. Introduction A normal physiologic response directly following birth is that the temperature of the newborn rises. If the newborn is immediately placed in a skin-to-skin position with the mother the temperature exhibits a more pronounced rise. The mechanism behind this is not known [1]. It is likely that maternal transfer of warmth to the baby plays an important role — in particular since the mother’s breast temperature also increases in response to skin-to-skin contact and breastfeeding [2]. During skin-to-skin contact maternal oxytocin levels rise and there is even a relationship between the intensity of the baby’s hand movements and oxytocin levels [3,4]. The rise of maternal temperature may activate sensory nerves in the infant. Such stimulation induces calm and relaxation by decreasing the sympathetic tone in the infant. One consequence of this is vasodilatation in the skin, which results in higher skin temperature. In a recent study by Bystrova et al. [1] the newborns’ skin temperature was measured in the axilla, interscapularly, and on the thigh and foot in response to skin-to-skin contact. It was found that the rise in skin temperature was especially pronounced in the feet. That supports the assumption that enhanced cutaneous vasodilatation plays an important role in the regulation of skin temperature. Whether the infant’s skin temperature rises also in response to skin-to-skin contact and breastfeeding later on during the perinatal period is not known. During the last decades in Sweden routines regarding normal childbirth have changed. The administration of epidural analgesia (EDA) has become a common intervention and in 2002, 39% of all primiparae received EDA at the clinic where the present study was conducted. Another common intervention at this clinic is to administer oxytocin (OT) infusion in order to augment labour. Fifty percent of all primiparaes who gave birth received this type of intervention [5]. Since these interventions have become widely accepted, there is an increasingly important need to investigate whether these interventions influence the physiology of the mother and infant immediately following birth and/or in the long-term. It has previously been demonstrated that EDA administration during labour may influence the temperature of the mother and her newborn. A rise (0.14 8C per hour) in maternal temperature was observed within the first hours following EDA treatment [6], and maternal fever was also observed during labour after EDA administration [7,8]. Other studies report an increase in the temperature of the fetus following in utero exposure to EDA [9]. A previous study performed by our group showed that the skin temperature of newborns whose mothers had been exposed to EDA and other kinds of pain relief was further elevated 45 min postpartum when compared to nonexposed infants [10]. Also, OT administration during labour has been shown to be followed by an increased fetal temperature [11]. There are no studies that have scrutinized the effects of EDA or OT administration during labour on the temperature of the newborn in connection with skin-to-skin contact and breastfeeding later on in the perinatal period. The aim of this study was twofold: to investigate (1) the skin temperature pattern in newborns two days after birth in
W. Jonas et al. connection to breastfeeding and to examine (2) if EDA administration and OT infusion during labour influence this parameter at this point in time.
2. Participants and methods 2.1. Study sample The study was conducted at one of the six maternity hospitals in Stockholm, Sweden. The mother—infant pairs were consecutively recruited on Mondays to Fridays during research weeks from January 2002 to December 2003. The hospital at which the study took place is located in an area with high educational level and good socio-economic status. However, the maternity routines do not differ from hospitals in the rest of Sweden. The following inclusion criteria had to be fulfilled: The mothers had to be Swedish speaking primiparae with an uncomplicated singleton pregnancy and a normal labour. The newborns had to be born at full term with an Apgar score of 8 or more at 1 min postpartum. The mother and her infant should not have been separated after birth not even for medical examinations. The newborns should have been exclusively breastfed and not been given any formula. The experiment was performed two days after birth. The mothers met the researchers about 10 to 24 h after delivery, when the research team (WJ or IW) informed the mothers about the ongoing study. The mothers were told that the researchers wanted to study some physiological and psychological parameters related to breastfeeding at 24—48 h after birth in mothers and infants. If the mother gave her written informed consent she was instructed to call for the researchers the next morning when the newborn showed signs of wanting to breastfeed (e. g. rooting, tongue movements). The mother—infant pairs were allocated to three groups depending on the treatments the mothers had received during and after labour: mothers who had received OT stimulation during labour (OT group, n = 9), mothers who had been exposed to EDA and OT infusion during labour (EDA group, n = 20), and mothers who had received neither EDA nor OT stimulation during labour (control group, n = 18). In total, 47 mother—infant pairs were included in the study. Fourteen mothers declined from participation. Of those, two mothers had received OT infusion during labour, 10 mothers had an EDA and OT infusion during labour and two mothers had no intervention at all.
2.2. Maternity routines after birth According to standard maternity routines, all healthy newborns are placed skin-to-skin with their mothers immediately after birth. The newborns remain on their mothers’ chests until the first breastfeeding is established or until the newborns fall asleep. Usually the partners of the women are present during and after childbirth. Rooming-in is practised. The maternity rooms are designed to facilitate an bat-home-feelingQ and to allow parents to interact with their newborn.
Infant temperature and breastfeeding
2.3. Experimental design All breastfeeding observations took place in the morning and were always conducted by the same two research midwives (WJ and IW). Before the experiment started, all newborns were lying with their clothes on in the bed of their mothers. The newborns were then undressed and were weighed having a diaper on. Thereafter a skin temperature electrode (Ellab, Copenhagen, Denmark; accuracy +/ 0.1 8C) was attached between the shoulder blades. Interscapular temperature measurements were chosen for practical reasons, in that placing an electrode between the shoulder blades was not only technically easier, it also avoided disturbing the breastfeeding behaviour of the infant. The newborns were then immediately placed skin-to-skin on the mothers’ chest and were covered with a light blanket in order to maintain body temperature. This procedure took 3 min. The first temperature recording was performed as soon as skin-toskin contact with the mother was established. Following this, interscapular temperature readings were performed at 5, 10, 20, and 30 min after skin-to-skin contact was established. The time of the onset as well as the duration of suckling was registered. If the breastfeeding finished before 30 min had passed, the mothers kept the newborns in their arms irrespective of breastfeeding. For the purposes of this study, the environmental temperature in the maternity rooms was monitored and found to vary between 22 and 24.4 8C.
2.4. Ethical considerations The study was approved by the Ethics committee, Karolinska Institute, Stockholm.
3. Statistical analysis For the statistical analysis of the data, the SPSS program (Statistical Package for the Social Sciences) version 12.0 was used [12]. The median (md) and interquartile distances Table 1
57 (Q25—Q75) were used to describe background variables and outcome data that were non-parametrically distributed. Temperature measurements are presented as means (m), standard errors of the mean (SE), and range (R). The mean values of temperature recorded at 10, 20 and 30 min were calculated. For testing temperature differences between the groups unpaired t-tests were used and to test the differences within the groups over time paired t-tests were used. To correlate newborn age to temperature the Pearson’s correlation coefficient was calculated. In order to test differences between the groups regarding background variables, the Mann—Whitney U-test for independent samples and the v 2 test were used for interval and category data, respectively. An exploratory multiple regression analysis was performed to study the impact of different background variables on the temperature differences in the first ten minutes of the observation period. Since the temperature recordings were only recorded every five minutes in the beginning of the study period, it is not possible to disentangle the effects on temperature of skin-to-skin contact and onset of suckling. In order to elucidate whether the temperature rise was due to skin-toskin contact or breastfeeding, the obtained temperature values were regrouped according to the onset of suckling. Some newborns started to suckle the breast within the first four minutes of the observation period. Thus, for those newborns the temperature obtained at skin-to-skin contact was also the temperature considered before the onset of suckling. In the newborns who started to breastfeed between five and nine minutes of the observation period, the temperature obtained at 5 min was considered as the temperature before suckling. For the newborns who started to suckle the breast between 10 and 20 min, the temperature recorded at 10 min was counted as the temperature before the onset of suckling. Those obtained temperature readings were then summarized and thus, a new variable bTemperature before the onset of sucklingQ was created. The first measurement of temperature following the onset of suckling in each individual was called bTemperature after the onset of suckling 1Q and the
Clinical characteristics of mothers and their newborns (median, Q25—Q75 and frequencies)
Maternal age (yrs) 1st stage of labour (h) 2nd stage of labour (min) Blood loss (ml) OT infusion before birth (h) Oxytocin before birth (ml) Oxytocin after birth (ml) Duration of EDA (h) Marcain (mg) Sufenta (Ag) Use of N2O (yes) Acupuncture (yes) Number of boys/girls Weight (g)
Control group (n = 18)
Oxytocin group (n = 9)
EDA group (n = 20)
p-value+
31 (27—33) 7.0 (4.5—9.4) 38 (28—60) 367.50 (260—500)
32 (28—33) 9.1 (8.4—11.0) 63 (43—70) 375 (237—850) 1 (0:50—4) 81.5 (32.25—164.75) 154.5 (23.25—450.75)
ns ns ns ns c) ns c) ns c) ns
10 5 8/10 3450 (3163—3751)
9 2 5/4 4030 (3252—4195)
31 (29—33) 11.1 (7.2—12.1) 35 (22—51) 490 (262—637) 1:45 (0:45—4:83) 95.5 (43—199) 340 (125—433.5) 3:37 (2:24—5:37) 22.5 (17.5—42.5) 12.5 (10—35) 17 6 11/9 3423 (3345—3725)
+ Comparisons (Mann—Whitney or v 2 test) were made between the a) control- and OT group, and b) control- and EDA group. If variables were empty in the control group, comparisons were made between the c) OT- and EDA group.
b) 0.05 ns ns a) 0.059
58
W. Jonas et al.
Table 2
Breastfeeding characteristics (median, Q25—Q75) at time of experiment
Neonatal age (h) Number of breastfeedings after birth Minutes from skin-to-skin contact to onset of suckling Breastfeeding duration (min) a
Control group (n = 18)
Oxytocin group (n = 9)
EDA group (n = 20)
p-valuea
36 (25—39) 7.5 (5—10.25)
36 (35—45) 6 (5—11)
33 (27—40) 6 (4.2—8.7)
ns ns
2 (1—9)
3 (0—12)
2 (1—5)
ns
30 (21—37)
22 (16—39)
21 (15—31)
ns
The Mann—Whitney test was computed between the control group and the study groups.
measurement obtained when all newborns had suckled the breast for five minutes or longer was called bTemperature after the onset of suckling 2Q.
4.4. Temperature pattern during skin-to-skin contact and breastfeeding
4. Results
During the first ten minutes of observation the temperature rose significantly in the control group (+ 0.91 8C, p = 0.001). The temperature remained at a plateau level (35 8C) during the rest of the observation period. A rise in temperature was also observed in the OT group in which the temperature increased by 1.47 8C ( p = 0.008) and remained stable around 36 8C. The EDA group showed a significant temperature decrease of 0.62 8C ( p = 0.019) during the first ten minutes, before remaining relatively stable (Table 3b; Fig. 1). When the mean values of the temperature recordings obtained at 10, 20 and 30 min were compared between the different groups the levels in the OT group were significantly higher than those of the control group ( p = 0.048). In contrast, the temperature of the EDA group did not differ from the control group (Table 3a).
4.1. Background data The obstetrical background data were collected from the maternity records. The clinical characteristics of mothers and their newborns and the outcome data of the breastfeed are documented in Tables 1 and 2. The only statistically significant difference between the groups was found regarding the use of N2O. The number of mothers who received N2O was greater in the EDA group compared with mothers of the control group ( p = 0.05). None of the mothers were smokers, and 75% of the mothers had a university degree.
4.2. State of the infants
4.5. Temperature in relation to the onset of suckling
All newborns were awake and hungry but calm before they started to suckle. None of the newborns cried.
4.3. Temperature at skin-to-skin contact When temperature recordings commenced the interscapular temperature of the newborns belonging to the control group was 34.19 C8. The temperature was initially slightly higher in the OT group (34,42 8C) than in the controls and the EDA group had the highest temperature (35,07 8C). The temperature in the EDA group was significantly higher than the temperature obtained in the control group ( p = 0.025) (Table 3a; Fig. 1). In the EDA group, the age of the newborn was negatively correlated to the mean temperature, indicating that the younger the infant the higher the temperature when the experiment started (r = 0.46, p = 0.04). Table 3a
For assessing the effect of suckling on temperature, the difference between the bTemperature before the onset of sucklingQ and bTemperature after the onset of suckling 1Q was calculated. The temperature rose significantly following the start of suckling in the control group (0.78 8C, p = 0.003), and also in the OT group (0.90 8C, p = 0.06). The temperature in the EDA group, however, did not increase significantly after onset of suckling (Table 3b; Fig. 2). Interestingly, the temperature in the newborns of the OT group started to rise immediately at skin-to-skin contact and not, as in the control group, after the onset of suckling. This suggests that an effect on temperature had occurred already as a response to skin-to-skin contact between mother and the newborn (Fig. 2). When the values bTemperature before the onset of sucklingQ and bTemperature after the onset of suckling 2Q
Newborn temperature data presented as mean, standard errors (SE) and range (R)
Differences in temperature between the following measurement Initial temperature Mean temperature (10—30 min)
Control group (CG) (n = 18)
Oxytocin group (OTG) (n = 9)
EDA group (EDA) (n = 20)
p-value
Mean
SE
R
Mean
SE
R
Mean
SE
R
CG/OTG
CG/EDA
34.19 34.94
0.26 0.28
3.5 3.70
34.42 35.86
0.3 0.34
1.90 2.92
35.07 34.69
0.26 0.29
3.30 4.13
ns 0.048
0.025 ns
P-values refer to differences between groups.
Infant temperature and breastfeeding
59
Figure 1 The interscapular temperature pattern (m, bars showing the standard error of the mean (SE)) of healthy newborns in the oxytocin (-E-), EDA group (-n-) and the control (-o-) during the first 30 min of a breastfeed day two postpartum. At b0Q skin-to-skin contact was established. A different temperature pattern was found in the three groups.
Figure 2 The interscapular temperature pattern of the oxytocin- (-E-), EDA- (-n-), and control- (-o-) groups when temperature values (m, bars presenting the standard error of the mean (SE)) were organized regarding the onset of suckling. A detailed explanation is given in the Statistics section.
were compared, the temperature in the control group continued to rise (0.96 8C, p = 0.001), but not in the other two groups (Table 3b). This suggests that the suckling stimulus has the function of a bsecond triggerQ on the temperature rise.
The only variable that showed a significant impact on the temperature difference was having an EDA ( p V 0.001). Altogether, these variables explained 64.6% of the variation in the temperature differences observed in connection to the onset of suckling ( p = 0.001).
4.6. Regression analysis To investigate the influence of other variables a multiple exploratory regression analysis was performed (Table 4). The dependent variable was bTemperature difference between skin-to-skin contact and temperature value at 10 minQ. The independent variables were 1) Oxytocin (0/1), 2) EDA (0/1), 3) oxytocin infusion before birth (ml), 4) duration of 2nd stage of labour (min), 5) acupuncture (0/ 1), 6) N2O (0/1), 7) neonatal age (h) at experiment, 8) number of breastfeedings after birth, and 9) neonatal weight (g) at birth.
Table 3b
5. Discussion The main findings in the present study were that breastfeeding two days after birth results in a rise in the interscapular temperature in infants and that the expression of this rise is dependent on whether or not the mothers received EDA and/or OT infusion during labour. One of the limitations of the study is that only interscapular temperature measurements were obtained.
Newborn temperature data presented as mean differences, standard error of the mean (SE) and range (R)
Temperature at skin-to-skin contact — temperature at 10 min Temperature before the onset of suckling — temperature after the onset of suckling 1 Temperature before the onset of suckling — temperature after the onset of suckling 2
Control group (CG) (n = 18)
Oxytocin group (OTG) (n = 9)
EDA group (n = 20)
Mean diff
SE
R
Mean diff
SE
R
Mean diff
0.91
0.2
3.1
1.47
0.37
2.7
0.78
0.20
2.8
0.90
0.38
0.96
0.21
3.1
0.70
0.45
p-value
SE
R
CG
OTG
EDA
0.62
0.22
2.4
0.001
0.008
0.019
2.7
0.18
0.19
2.4
0.003
0.06
ns
3.1
0.33
0.23
2.3
0.001
ns
ns
P-values refer to differences over time within each group as calculated below.
60 Table 4
W. Jonas et al. Regression analysis
Model
B-coefficient
SE
Constant Oxytocin (0/1) EDA (0/1) Acupuncture (0/1) Use of N2O (0/1) OT before birth (ml) Duration 2nd stage of labour (min) Neonatal weight (g) Neonatal age (h) Number of breastfeedings since birth
0.795 0.360 1.697 0.538 0.673 0.081 0.000 2.334E 05 0.019 0.067
1.569 0.574 0.408 0.363 0.376 0.151 0.000 0.000 0.025 0.062
t-value 0.507 0.628 4.160 1.482 1.789 0.091 0.138 0.009 0.125 0.177
p-value 0.617 0.536 0.000 0.151 0.086 0.598 0.343 0.946 0.448 0.294
Dependent variable: temperature difference between the temperature at 10 min and skin-to-skin contact (df = 9, R 2 = 64.6%, Adjusted R 2 = 51.9%, overall significance p = 0.001).
However, in earlier studies conducted by our group the interscapular temperature of the newborn was measured [1,10,13]. Those studies showed that the interscapular temperature values correlated well with temperature measurements obtained at other parts of the body, i.e. the axilla, thigh and foot. Another limitation of the study is that randomization of mothers before birth to either OT infusion or EDA treatment is impossible for practical and ethical reasons. However, our participants were consecutively selected following strict inclusion criteria. The participants were derived from a very homogenous group of women suggesting that the material is representative for the use of the interventions at the clinic where the study was performed. It is well known that infants’ temperature naturally increases postpartum [10,13]. If the baby is placed in skinto-skin contact with the mother the temperature exhibits a further rise [1]. Our novel finding of a rise of newborns’ skin temperature during breastfeeding and skin-to-skin contact two days after birth suggests that the infant responds in a similar way at this point in time as when being placed skin-to-skin immediately postpartum. After birth the infant is exposed to lower environmental temperatures and sympathetic fibers innervating the brown fat tissue are activated and heat is generated through lipolytic processes [14]. It is also known that heat production increases after ingestion of a meal in infants [14]. Whether skin-to-skin contact and suckling trigger also heat production by increasing lipolytic processes is not known, but remains a possibility [14]. However, the degree of vasodilatation in cutaneous blood vessels is of importance for the temperature recorded in the skin. Therefore, variations in the balance between cutaneous vasoconstriction and vasodilatation will also be of importance for the temperature levels obtained [2,15]. In a recent study we were able to show that the rise of infants’ skin temperature postpartum was dependent on maternity routines. The foot temperature for example exhibited a clear rise in response to skin-to-skin treatment and a fall after separation from the mother [1]. The exaggerated rise of foot temperature in the skin-to-skin group suggests that part of the increase in temperature is due to a change in the autonomic nervous tone resulting in reduced sympathetic nerve activity and consequent cutaneous vasodilatation.
The stress of being born is accompanied by an increased activity in the sympathetic nervous system, peripheral vasoconstriction and a reduction in skin temperature [16]. In contrast, touch and warmth, as during skin-to-skin contact activate cutaneous sensory nerves which lead to a reduction of the sympathetic nervous tone [17]. Consequently, peripheral circulation is enhanced, which is followed by an increased skin temperature in e.g., the foot [1]. Touch and warmth applied on the chest are particularly powerful stimuli to antagonize stress, due to the presence of a particular kind of afferent nerves originating from this area [18]. In addition to the sensory fibers innervating the spinal cord, these signals reach the CNS via the ganglion nodosum and the nucleus tractus solitarius (NTS) [15,18]. There is a direct connection between the NTS and the oxytocinergic nerves in the paraventricular nucleus (PVN). The oxytocinergic nerves emanating from the PVN subsequently reach many regulatory areas in the brain. OT exerts inhibitory effects on sympathetic nervous tone and the release of OT may therefore contribute to the antistress effect exerted by bnon-noxiousQ sensory stimulation of the skin, in particular if triggered from the ventral side of the chest. OT has been shown to be released both into the circulation and into the CNS in response to warmth and touch in a rat model [19]. No such direct observations have been done in humans. However, suggestive evidence for the release of OT in the CNS is provided by two studies showing a relationship between personality changes and the levels of OT in connection with breastfeeding [20,21]. In addition to skin-to-skin contact, suckling also induces activation of vagal nerve afferents, which may be followed by an enhanced vagal tone and antistress effects of the type described above as induced by skin-to-skin contact [22]. Therefore, the rise of infants’ interscapular skin temperature during breastfeeding two days after birth may be related to suckling, as well as to skin-toskin contact. However, our data showing that the rise of temperature had started before the onset of suckling in the OT group suggests that the skin-to-skin contact was an important factor in triggering these responses. Unfortunately, due to the design of the study, it is not possible to disentangle the effects caused by skin-to-skin contact per se and suckling. The medical interventions applied to the mother during labour influenced the temperature response. In those
Infant temperature and breastfeeding infants whose mothers had received an OT infusion during labour, the response was exaggerated. Possibly OT is responsible for these effects. In order to induce these effects OT has to reach the CNS of the infant. Malek et al. [23] scrutinized both the maternal—fetal and the fetal—maternal placental diffusion of OT in vitro and found that more OT is transferred to the fetus than back to the mother. Thus, OT infusion given during labour could reach the circulation of the fetus and may thus induce the effects in response to OT infusion as observed in the present study. A limited percentage of exogenous OT passes the blood— brain barrier of adult animals [24,25]. However, since the blood—brain barrier is not fully developed in the neonatal period under consideration larger amounts may enter the CNS at this age. This opens up for the possibility that maternal OT infusion during labour may reach the brain of the fetus to induce effects observed in the present study. Results from animal experiments show that repeated exposure to OT in the postnatal period gives rise to lifelong effects. These effects include antistress-like effects, such as the lowering of blood pressure [26] and corticosterone levels [22], an increased pain threshold and weight gain [27]. The effects are sometimes not apparent until adulthood [28,29]. The effects of skin temperature in the infant observed in the present study may be a consequence of an altered autonomic nervous balance. A higher parasympathetic nervous tone may be related to increased circulation in the skin and hence a higher temperature. In those infants whose mothers received EDA during labour the initial temperature was higher and the consequent rise of temperature during breastfeeding was abolished. EDA is known to enhance the temperature in mothers during labour and in both mothers and infants after birth [6— 9]. The effects have been suggested to be a consequence of an influence on the center of temperature regulation both in mothers and infants [30]. The reasons for this are unknown. The higher initial temperature recorded in infants having been exposed to EDA in the present study may reflect a remaining effect of an early disturbance of the temperature regulation. This assumption is supported by the fact that the initial temperature obtained in infants of the EDA group was inversely related to age of these infants; in other words, the higher the temperature, the younger the infant. The second finding that infants from the EDA group did not display a rise of temperature in response to breastfeeding is more difficult to explain. Hypothetically, the effect might be due to decreased levels of OT in the brain of the infant. EDA is known to decrease OT levels during labour but the mechanism behind this effect is not fully understood. One possibility is that the EDA, when blocking the activity from the afferent nerves from the uterus, not only blocks the transmission in nerve fibers mediating pain but also those mediating OT release into the maternal circulation and brain which might lead to a reduction of OT levels. Another possibility that must be considered is that the opioid component of the EDA inhibits OT release. Opioids are known to inhibit the release of OT [31]. Sufentanil, which was used in the present study, may leak out into the maternal circulation and decrease OT release. The brain of the infant may however also be influenced directly by
61 sufentanil, since this substance is highly fat-soluble and has been shown to cross the placental barrier by passive diffusion, to accumulate in placental tissue, and to reach the circulation of the infant [32]. It also quickly penetrates the blood—brain barrier. Even though levels of sufentanil are very low in the umbilical blood vessels it is likely that they could still influence the newborns’ brain [33]. If so, not only maternal OT release but also that of the infant may be inhibited during and after birth, as long as the active metabolites are still present in the circulation. Assuming that the EDA by various mechanisms reduces the infant’s OT levels during a very critical period of life, the attunement of the autonomous nervous tone normally occurring at this point of time might be influenced. The lack of a temperature change during breastfeeding two days after birth might be an expression of this. An intriguing and compelling question is whether relative reduction in OT exposure during the perinatal period not only produces changes in thermoregulation some time after birth but may also influence cardiovascular function and pain. It is important to notice that the above-mentioned results are preliminary and that the explanations still remain speculative. Further studies are needed to corroborate the findings since the effects observed for the labour ward interventions on the skin temperature of the newborn may be due to completely different, and as yet unknown, factors. However, if the effects described above are, in fact, consequences of labour ward routines, it is of immense importance to demonstrate and describe them in detail since the manifestations of these effects in particular may become more pronounced in adulthood. Given the large numbers of women receiving these treatments, even minor effects on newborns might have important future physiological and behavioural consequences for the human population.
Acknowledgments The authors would like to thank all mothers and newborns participating in this study and the staff at BB-Stockholm. Also, we would like to thank the Va ˚rdal Stiftelsen, the Swedish Research Council (K 1999-2001 27P-13085 and K 1999-27XP-13263-01), the Centre for Health Care Sciences at the Karolinska Institute and Praktikertja ¨ nst AB for research grants.
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