Published online November 1, 2005
PEDIATRICS Vol. 116 No. 5 November 2005, pp. 1105-1113 (doi:10.1542/peds.2004-2440)
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Salivary Cortisol and Mood and Pain Profiles During Skin-to-Skin Care for an Unselected Group of Mothers and Infants in Neonatal Intensive Care

Evalotte Mörelius, RN, MS*, Elvar Theodorsson, MD, PhD{ddagger} and Nina Nelson, MD, PhD*

* Department of Molecular and Clinical Medicine, Division of Pediatrics
{ddagger} Department of Biomedicine and Surgery, Division of Clinical Chemistry, University Hospital, Linköping, Sweden


   ABSTRACT
TOP
 ABSTRACT
METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Objectives. Mother-infant separation after birth is a well-known source of stress. Parents and preterm infants in neonatal intensive care are separated immediately after birth. Skin-to-skin care is 1 possible method to reduce the separation-dependent stress. The aim of the present study was to investigate how skin-to-skin care influences stress for the mother and the infant in neonatal intensive care.

Methods. Seventeen mother-infant pairs were included at their first and fourth skin-to-skin care. The infants were 25 to 33 weeks' gestational age, with birth weights ranging from 495 to 2590 g. In mothers, salivary cortisol, heart rate, mood scale, and stress measured on a visual analog scale (VAS) were analyzed. In infants, salivary cortisol and heart rate were analyzed, and because pain is one facet of stress, 2 different pain scales were used.

Results. In mothers, the skin-to-skin care decreased salivary cortisol (32%), heart rate (7%), and VAS (89%), whereas mood increased (6%). Before the fourth skin-to-skin care, mothers rated less stress on VAS, and salivary cortisol and heart rate improved faster. The infants' cortisol either increased or decreased. Their heart rates and pain scores decreased during skin-to-skin care.

Conclusions. Our results lend additional support to the value of skin-to-skin care in neonatal intensive care. Variable stress responses in preterm infants favor the need for individualized care. The mothers' need for support seem to be more pronounced in the first skin-to-skin session as our results show a higher degree of stress as compared with later skin-to-skin care.

Key Words: cortisol • newborn infant • maternal behavior • pain measurement • stress

Abbreviations: SSC, skin-to-skin care • SaO2, oxygen saturation • VAS, visual analogue scale • PIPP, Premature Infant Pain Profile • NIPS, Neonatal Infant Pain Scale • Fr, Friedman statistical test • Wi, Wilcoxon signed ranks tests

Infants in NICUs are commonly exposed to painful and stressful situations, which are inherent in this special type of medical care.1,2 When the infant attempts to cope with a stressful situation, the developing hypothalamic-pituitary-adrenal axis is activated, culminating in alterations of plasma cortisol levels.3 A recent study by Grunau et al4 showed that extremely preterm infants have a different pattern of cortisol response at 8 months' corrected age as compared with term infants. They found a correlation between procedural pain exposure in preterm infants and increased cortisol at 8 months' corrected age. Long-term side effects of high concentrations of cortisol can result in insulin resistance, hyperlipidemia, immunologic deficiencies, and destructive changes in the hippocampus.3,5–7 It therefore is essential to minimize pain and to identify which interventions in NICUs reduce stress in both infants and parents and to prioritize these interventions in everyday care.

Kangaroo, or skin-to-skin care (SSC), is a widely used and approved method of interrupting the separation between the infant and the parents as a result of incubator care during intensive care.8 Several studies show that physiologic parameters such as heart rate, oxygen saturation (SaO2), and temperature regulation remain stable for the infant during SSC.9,10 Even an intubated infant can be cared for safely during SSC.11,12 SSC is shown to be analgesic for term healthy infants while they undergo a standard heel-lance procedure.13 However, there are no studies on the effect of SSC on stress hormone responses together with complete pain profiles in preterm infants; neither are there any reports on the effect of SSC on stress hormone responses and mood changes for the parent.

Since Francis et al in 198714 showed a correlation between infants' plasma and saliva cortisol, only a few studies that have investigated salivary cortisol in preterm infants during procedures have been published, basically as a result of methodologic problems.15–19 However, a new method to collect and analyze cortisol in small amounts of saliva was published recently.20 It thereby is possible to collect sufficient amounts of saliva without disturbing the infant, for instance during sensitive situations as mother-infant interaction.

The primary aim of the present study was to investigate how SSC influences indicators of stress in the mother and her infant as measured by salivary cortisol and mood changes. A secondary aim was to investigate whether there is a difference in the stress response between the first and a later SSC, which we chose to be the fourth session, when the mother may have adapted to the situation of caring for her preterm infant skin to skin.


   METHODS
TOP
 ABSTRACT
 METHODS
RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Design
It is well known that infants, in contrast to adults, do not have a diurnal rhythm of cortisol.21,22 It therefore is essential to have a study design that is suitable to this condition. A baseline response–paired design was used, all individuals acting as their own controls before, during, and after SSC on 2 different occasions (first SSC and fourth SSC). The time for the first SSC was decided together with the mother and the staff members on the basis of the infant's schedule for the day. The fourth SSC was performed at the same time of the day as the first SSC to match the diurnal variation of cortisol for the mother.

Setting
The study was conducted in the NICU, a tertiary unit at the University Hospital, Linköping, Sweden. The NICU is a 17-bed, Newborn Individualized Developmental Care and Assessment Program–influenced setting23 with ~450 newborns a year, including infants with minor medical problems. It is a standard practice that all mothers and/or fathers are holding the infant skin to skin as soon as the infant is considered medically stable to handle the transition from the incubator to the parent. An SSC session usually lasts for at least 1 hour and is interrupted only if the infant is getting medically unstable.

Inclusion Criteria
Preterm infants who were aged 2 days or older and cared for in an incubator and had no previous SSC were considered for the study. The infants had to be 2 days old to have stabilized their cortisol levels after birth.24 Infants with congenital anomalies, intraventricular hemorrhage, or neurologic impairment were excluded. The participating mothers had to be fluent in Swedish, as this was crucial for obtaining reliable results using the questionnaires. When the mother and the infant's nurse had agreed on a time for SSC, the mother was orally informed about the study and asked whether she wanted to participate. She was also given written information about the study. The local ethics committee approved the study, and informed consent was obtained from all participating mothers.

Participants
Seventeen mother-infant pairs were included in the study between October 2001 and November 2003. Most infants who were in the NICU during the study period had SSC before they were 2 days old and therefore could not be included in the study. Because of ethical issues, we chose not to interfere with the standard practice of the unit, thus not restraining them from having SSC when eligible. Two families did not consent to participate because (1) 1 mother was personally acquainted with 1 of the authors, and (2) 1 father wanted to participate but not the mother in question. The mothers had a mean age of 29 years (range: 22–37 years). One mother had rheumatoid arthritis, another had allergy, and 1 had essential tremor, but they all were doing well without medication at the time of the investigation as well as during the pregnancy. All of the mothers were married or living with the infant's father. Eleven of the mothers were primiparous (Table 1). The infants all were preterm (25–33 weeks), with birth weights ranging from 495 to 2590 g. At the time of the first SSC, the infants were 2 to 21 days of age. Sixteen of the infants were on continuous positive airway pressure, and 1 was on a ventilator. Six of them had supplemental oxygen (Table 2). Three mother-infant pairs did not participate in the second study session (fourth SSC) because they were already discharged from the University Hospital and referred to their home county hospitals (Tables 1 and 2).


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  		TABLE 1. Clinical Data of Participating Mothers During First and Fourth SSCs

 

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  		TABLE 2. Clinical Data of Infants During First and Fourth SSCs

 
Salivary Cortisol
Saliva was collected from mothers and infants using cotton-tipped applicators, as described previously.20,25 Because several components can confound salivary cortisol measurements, the mother was told not to eat, drink, smoke, or exercise 1 hour before the study session. All infants were fed through a nasogastric tube, and their mouths were checked gently for any contaminating components before saliva collection. After collection, the saliva was frozen immediately and stored at –22°C. A radioimmunoassay for cortisol was used to analyze cortisol concentrations in saliva.20 Intra-assay coefficients of variation were 12% at 2.0 nmol/L and 6.0% at 10.0 nmol/L. Samples were run neat in duplicate, and all samples from an individual were run in the same assay.

Stress and Mood Profiles: Mothers
The mood scale,26 a self-administered instrument, was used to measure the bipolar dimensions of mood in mothers. The instrument consists of 71 adjectives measured on a 4-point scale (1 = it definitely disagrees with what I feel right now, 4 = it definitely agrees with what I feel right now). The adjectives are, for instance "secure," "relaxed," "attached," "happy," "energetic," and "sociable." The adjectives are divided into 6 dimensions (control, calmness, social orientation, pleasantness, activation, and extraversion). The dimensions are analyzed separately as well as total sum mean score with a minimum and maximum of 12 and 47, higher values indicating a better mood. The mood scale is available as a computerized version, ie, the participant responds by pressing predefined buttons on a laptop; the procedure takes 3 to 5 minutes. The mood scale has been used previously in several intervention studies.27–29 The visual analog scale (VAS) is an internationally accepted method for measuring subjective emotions.30 In the present study, we used the VAS to have the mothers grade their stress by placing a marker somewhere between "no stress at all" and "worst stress imaginable." The opposite side of the scale (seen only by the researcher) is marked with numbers from 0 (no stress at all) to 100 (worst stress imaginable). Mothers' heart rates were measured by palpating the radial pulse for 1 minute.

Pain Profiles: Infants
The Premature Infant Pain Profile (PIPP)31 and the Neonatal Infant Pain Scale (NIPS)32 were used to measure pain bedside. PIPP comprises 3 behavioral variables (time of brow bulge, eye squeeze, and naso-labial furrow), 2 physiologic variables (changes in heart rate and Sa2), and 2 contextual variables (gestational age and behavioral state). Behavioral state ranges from "active/awake, eyes open, facial movements" to "quiet/sleep, eyes closed, no facial movements." Every variable is scored on a scale from 0 to 3. Minimum PIPP score is 0 (no pain), and maximum score is 21. The heart rate and Sa2 were measured with a cardiorespiratory monitor (Hewlett Packard, Böblingen, Germany). NIPS comprises 5 behavioral variables (facial expression, cry, arm movements, leg movements, and behavioral state) and 1 physiologic variable (breathing pattern). Every variable is scored on a scale from 0 to 1 or 2 (cry). Minimum NIPS score is 0 (no pain), and maximum score is 7. PIPP and NIPS have documented reliability and validity and have been used previously in several studies of pain in preterm and term neonates.31,32

Procedure
The investigation was performed the first time the infant was taken out of the incubator for SSC and repeated the fourth time the infant had SSC with the mother. The mother was instructed to dress in a hospital gown that opened down the front and to sit comfortably in a reclining chair with a footrest especially used in kangaroo care. The sequence of first data collection (pre-SSC) was always the same: the mother rated VAS, heart rate was measured, and saliva was collected from the mother. The mother was asked to complete the mood scale on a laptop placed on her knee. The PIPP and NIPS were rated for the infant, and saliva was collected. Thereafter, the infant was removed gently from the incubator and placed on the mother's chest in an upright position. The infant was wearing a cap and a diaper. She or he was placed inside the mother's hospital gown with extra blankets on top. The mother was provided with a mirror to see the infant's face. The father was sitting on a chair near the mother-infant pair. A folding screen was placed in front of the family to ensure their privacy. The room that was used for SSC is a 4-bed intensive care room with 3 windows. The Venetian blinds were closed, and the room was kept dark; the staff kept their voices low.23 When the mother-infant pair had rested skin to skin for 30 minutes, the second data collection (during SSC) was performed. The second data collection always followed the same sequence: starting with PIPP and NIPS for the infant; then VAS, heart rate, and saliva collection for the mother; saliva collection from the infant; and finally the mood scale for the mother. The mother completed the mood scale on the laptop (held by the father in all cases but 1, when 1 of the staff members helped the mother) with 1 hand while she held the infant firm with her other hand, still resting in the reclining chair. After the second data collection was completed, the mother and the infant rested for another 30 minutes. During the whole session, heart rate, Sa2 and behavior were observed and recorded for the infant along with environmental factors in the room. The room during SSC was graded as either calm (normal) or noisy (extraordinary activity/noise in the room, eg, other infant crying; procedures performed with other infants; >4 staff members in the room). When the SSC was completed, the child was removed gently from the mother's chest and replaced in the incubator. Thirty minutes after the mother-infant separation, the research procedure was repeated according to the same sequence as pre-SSC. The same investigator (E.M.) performed all ratings (PIPP, NIPS, and heart rate).

Statistics
Data were analyzed using the statistical software SPSS (version 11.5). Friedman (Fr) and Wilcoxon signed ranks tests (Wi) were used to analyze differences in paired data. Fisher's exact test, a {chi}2 test (exact significance, 2-sided) was used to analyze changes in cortisol (increases/decrease in cortisol during SSC) with environmental factors (calm/noisy) and SSC with father between first and fourth SSC with mother (yes/no). In some cases, data were missing because of insufficient amount of saliva. When data were missing, the infant was excluded from paired analyses but included in other nonpaired analyses. Therefore, the numbers of subjects for each analysis may differ slightly.


   RESULTS
TOP
 ABSTRACT
 METHODS
 RESULTS
DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Mothers
Salivary Cortisol
Saliva samples from all 3 occasions (pre-SSC, SSC, and post-SSC) were eligible for analysis for all mothers (n = 17) at the first SSC. The highest cortisol levels for the first SSC were detected pre-SSC and the lowest post-SSC. The median post-SSC cortisol level was 32% lower than the pre-SSC level (P = .002, Fr/Wi) and 27% lower than during SSC (P = .01, Fr/Wi; Fig 1). Saliva samples from all 3 occasions (pre-SSC, SSC, and post-SSC) were eligible for analysis for all mothers (n = 14) at the fourth SSC. The median cortisol level for mothers at the fourth SSC was highest pre-SSC and lowest post-SSC. The median SSC level was 22% lower than the pre-SSC level (P = .01, Fr/Wi). The median post-SSC cortisol levels were 38% lower than the pre-SSC levels (P = .03, Fr/Wi) and 20% lower than during SSC (P = .02, Fr/Wi). No significant differences were found between the first and the fourth SSC in the mothers' cortisol levels (Fig 1).


Figure 1
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  		Fig 1. Salivary cortisol, VAS score, total mood scale score, and heart rate for mothers before, during, and after the first and fourth SSCs. {circ}, outliers.

 
VAS
The highest VAS score for the first SSC was rated pre-SSC and the lowest post-SSC. The VAS decreased 81% during SSC (P = .002, Fr/Wi) and 89% post-SSC (P = .001, Fr/Wi) compared with pre-SSC (Fig 1). The median VAS score for mothers at the fourth SSC was highest pre-SSC and lowest post-SSC. The VAS decreased 65% (P = .003, Fr/Wi) during SSC and 83% post-SSC (P = .02, Fr/Wi) compared with pre-SSC. Mothers rated 6% higher stress levels (P = .04, Wi) before the first SSC compared with before the fourth SSC (Fig 1).

Mood Scale
Total mood scale scores for mothers at the first SSC were highest during SSC and lowest pre-SSC. The median SSC mood scale score was 6% higher than pre-SSC (P = .003, Fr/Wi), and post-SSC was 5% higher than pre-SSC levels (P = .04, Fr/Wi; Fig 1). Three of the 6 mood scale dimensions (control, calmness, and pleasantness) increased significantly during SSC (P = .001, .001, and .03, respectively, Fr/Wi). The dimensions control and calmness increased post-SSC compared with pre-SSC (P = .02 and .003, respectively, Fr/Wi). The total mood scale scores for mothers at the fourth SSC were highest post-SSC and lowest pre-SSC. However, the changes in mood scale score during the fourth SSC did not reach statistical significance. There were no significant differences in mothers' moods between the first SSC and the fourth SSC (Fig 1).

Heart Rate
The median heart rate at the first SSC was highest pre-SSC. The median heart rate decreased 7% post-SSC compared with pre-SSC (P = .03, Fr/Wi; Fig 1). The median heart rate at the fourth SSC was highest pre-SSC. The heart rate decreased 6% during SSC (P = .007, Fr/Wi) and 7% post-SSC (P = .004, Fr/Wi) compared with pre-SSC. There were no significant differences between mothers' heart rates on the first SSC compared with the fourth SSC (Fig 1).

Infants
Salivary Cortisol
At the first SSC, 43 (84%) of 51 samples contained sufficient volumes for analysis. Among those, 3 had to be excluded because of blood contamination, thus making 40 (78%) samples eligible for analysis (Fig 2). Samples from all 3 occasions (pre-SSC, SSC, and post-SSC) were eligible for analysis in 12 (70.6%) cases and for 2 occasions (pre-SSC and SSC) in 1 case (Fig 3). Thirty-eight percent (n = 5) of the infants decreased in cortisol concentrations during SSC, and 38% (n = 5) increased in cortisol concentration during SSC. Twenty-three percent (n = 3) neither increased nor decreased in cortisol. The median cortisol level at the first SSC was highest post-SSC and lowest pre-SSC. The changes in cortisol during and after SSC did not reach statistical significance (Fig 2). The change in cortisol levels during first SSC did not depend on whether the environment was calm or noisy (P = .657, Fisher's exact test).


Figure 2
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  		Fig 2. Salivary cortisol, heart rate, and NIPS and PIPP scores for infants before, during, and after the first and fourth SSCs. {circ}, outliers.

 

Figure 3
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  		Fig 3. Salivary cortisol values for infants before, during, and after the first SSC. Each line represents 1 individual; the y-axis is logarithmic.

 
At the fourth SSC, 40 (95%) of 42 samples contained sufficient volumes for analysis. Among those, 3 had to be excluded because of blood contamination, thus making 37 (88%) samples eligible for analysis (Fig 2). Samples from all 3 occasions (pre-SSC, SSC, and post-SSC) were eligible for analysis in 11 (78.6%) cases. In 2 cases, samples were eligible for analysis from 2 occasions (SSC and post-SSC, and pre-SSC and post-SSC, respectively; Fig 4). Thirty-six percent (n = 4) of the infants decreased in cortisol concentrations during SSC, and 64% (n = 7) increased in cortisol concentrations during SSC. The median cortisol level at the fourth SSC was highest post-SSC and lowest pre-SSC. Salivary cortisol was 60% higher pre-SSC (P = .007, Wi) at the first SSC compared with the fourth SSC and 47% higher post-SSC (P = .03, Wi) at the first SSC compared with the fourth SSC (Fig 2). Seven infants had SSC with the father between the first SSC and the fourth SSC. Alteration in cortisol during the fourth SSC was not related to SSC with the father between the first and fourth SSCs (P = .183, Fisher's exact test) or to environment classification as calm or noisy (P = .491, Fisher's exact test).


Figure 4
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  		Fig 4. Salivary cortisol values for infants before, during, and after the fourth SSC. Each line represents 1 individual; the y-axis is logarithmic.

 
Heart Rate
The median heart rate at the first SSC was highest pre-SSC (153; minimum/maximum: 137/177) and lowest during SSC (145; minimum/maximum: 127/168). The heart rate decreased 5% during SSC (P = .007) and 4% post-SSC (P = .03, Fr/Wi) compared with pre-SSC (Fig 2). The median heart rate at the fourth SSC was highest post-SSC (156; minimum/maximum: 133/184) and lowest during SSC (146; minimum/maximum: 131/186). The heart rate decreased 4% during SSC (P = .04, Fr/Wi). The heart rate increased 7% post-SSC compared with SSC (P = .009, Fr/Wi). There were no significant differences in heart rate between the first and fourth SSCs (Fig 2).

NIPS
The highest median NIPS score at the first SSC was registered pre-SSC. There was a significant decrease in the NIPS during SSC compared with pre-SSC (P = .005, Fr/Wi). There was also a significant decrease post-SSC compared with pre-SSC (P = .04, Fr/Wi) and a significant increase post-SSC compared with during SSC (P = .04, Fr/Wi; Fig 2). The highest NIPS score at the fourth SSC was noted pre-SSC and the lowest during SSC. There was a significant decrease in the NIPS during SSC compared with pre-SSC (P = .03, Fr/Wi). There were no significant differences in the NIPS between the first and fourth SSCs (Fig 2).

PIPP
At the first SSC, there was a significant difference in behavioral state pre-SSC compared with during SSC (P = .046, Fr/Wi). The median behavioral state pre-SSC was 2, ie, "active/sleep, eyes closed, facial movements." The median behavioral state during SSC was 3, ie, "quiet/sleep, eyes closed, no facial movements." There were no differences in total PIPP scores at the first SSC (Fig 2). At the fourth SSC, the children were more in the state "quiet/sleep, eyes closed, no facial movements" during SSC compared with pre-SSC, but the difference was not significant. There were no significant differences in PIPP or behavioral state between the first and fourth SSCs (Fig 2).


   DISCUSSION
TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
CONCLUSIONS
 REFERENCES
 
A preterm infant who is admitted to a NICU and placed in an incubator immediately after birth is separated from his or her parents, and the family experiences the stress of physical separation.33 The most important negative stressor reported by mothers in this situation is the separation from their infants, especially not being able to hold them.34 Our results show that mothers experience a high degree of stress and low mood indicators (especially control, calmness, and pleasantness) before the first SSC. Self-rated stress (VAS) decreased and mood improved significantly when they held their infants skin to skin. Salivary cortisol and heart rate also decreased during SSC, but the change reached significance only after the SSC was completed. These findings may indicate that it was only after having managed the entire SSC session that the mother was able to relax completely. Before and during the first SSC, the mother is unfamiliar with the new unpredictable situation, experiences low control and calmness, and has difficulty coping with the situation.35 Furthermore, the mother is likely to be afraid of harming the infant, because she does not know how much the infant can handle.34

At the fourth SSC, the mother has adapted to the situation: she knows the procedure, what to expect, and the infant's abilities. Consequently, her self-rated stress (VAS) is not as high before the fourth SSC as before the first SSC, and her salivary cortisol and heart rate start to decrease already during the SSC. Positive feelings have previously been shown to lower cortisol concentrations,36 and other studies that have investigated SSC reported increased experience of pleasure by the mothers.37,38 However, no one has previously reported the relationship between SSC and the mothers' cortisol response shown in the present study.

Our results show that cortisol concentrations in infants, in contrast to their mothers, may increase as well as decrease during SSC. The increase in cortisol levels could be a sign of stress.39,40 However, that the PIPP and NIPS decreased along with the heart rate during SSC suggests that the increase as well as the decrease of cortisol concentrations may be a result of an immature control of the hypothalamic-pituitary-adrenal system.41–43 Similar results have been described previously when massage as an intervention either increased or decreased cortisol in infants.16,44 Smyth et al36 found that adults with normal cortisol cycles had a large cortisol response to stressors, whereas adults with "inconsistent" cycles had no or negative cortisol response. Gitau et al16 also studied preterm infants during SSC and found that salivary cortisol decreased during SSC. However, in contrast to our study, the infants in their study were no longer in intensive care, and it is unclear whether they had had SSC before the investigation or not. It is interesting that in our study, the cortisol was significantly higher at the first SSC than at the fourth SSC, when the infants were clinically more stable. The postnatal age influences the maturation of the diurnal rhythm of cortisol. Although the infants in our study are too young to have a diurnal rhythm,21,22 the lower and somewhat more stable cortisol values at the fourth SSC as was shown with paired statistics (Wi/Fr) could be an effect of postnatal age, maturation, or clinically more stable infants. Nevertheless, salivary cortisol responses in preterm infants are difficult to interpret and need to be explored further.

Because there was a decrease in NIPS on both occasions, this could mean that the infants were more comfortable and well supported by the mothers skin to skin than in the incubator. The infants are exposed to positive human touch45 on a larger area of the body than when in the incubator wrapped in a nest. Furthermore, they are able to hear the mother's heartbeat, which has previously been shown to reduce infant stress.46 The infants were more relaxed and had a deeper sleep during both the first and the fourth SSC as reflected by their heart rate and behavioral state, a finding supported by earlier studies.47,48 We know from other studies that there is no correlation between behavioral state and cortisol in infants.14,49 SSC, however, seems to have positive effects on neurobehavioral responses of the infant. One newly published study showed that kangaroo care can help term infants to regulate themselves in terms of motor system balance and sleep organization.50 Preterm infants in intensive care, however, have a more immature motor system and have larger difficulties in self-regulation.23 Although the body temperature is known to effect the heart rate, it was not controlled for during SSC, because earlier studies confirmed that the core temperature remains stable during SSC.9,10,38

The PIPP and NIPS are instruments that have been validated to measure pain rather than stress.31,32 Pain, however, is 1 important facet of stress in the newborn, and it is difficult or perhaps even impossible to distinguish stress from pain. We used 2 different instruments that were designed to measure pain in the present study along with salivary cortisol; thereby, we have measured successfully several separate facets of stress in the newborn. The correlation between salivary cortisol and different pain scales needs to be investigated further to find a clinically practical bedside instrument to evaluate stress in preterm infants and to learn more about stress physiology in the newborn.

Many investigators have previously pointed out the advantages of using salivary cortisol as a marker of stress in adults,51 children,52 infants,14,25 and preterm infants.53 Measuring cortisol in saliva rather than in plasma or urine has several advantages besides that concentrations of cortisol in the saliva reflect the free cortisol concentration in plasma; the sampling procedure is painless, noninvasive, and performed easily.20 Although the saliva method is so advantageous, only a few studies have been published on preterm infants' cortisol responses during procedures at early ages.15–19 Even fewer studies included infants who were <30 weeks' gestation.16,18 One reason for this is that it is difficult to obtain sufficient amounts of saliva from preterm infants. Furthermore, saliva stimulants such as citric acid may interfere with the analysis of cortisol.54 Gitau et al,16 for instance, used citric acid to stimulate salivary flow in preterm infants and purified the samples before analysis. Despite this, they did not achieve sufficient amounts of saliva. Similar problems were addressed in other studies that included preterm infants.15,17–19 Herrington et al,19 for instance, included 8 preterm infants, and only 46% of their saliva samples yielded sufficient amounts of saliva. We have explored the essence of a kangaroo session as it is performed in our NICU. The kangaroo procedure and the context are the same for all infants. Although it is difficult to obtain sufficient amounts of saliva from preterm infants, we managed to collect saliva from infants at 2 different occasions and at 3 times at every occasion with a high success rate without using salivary flow stimulants.

Our intention from the onset was to include both mothers and fathers in the study. Unfortunately, we had to make do with mothers only as most fathers refrained, wanting the first time to be exclusively for the child's mother. However, in all but 1 case, the fathers observed the whole session. Randomizing the first session between the mother and the father was not considered ethical or in line with our main purpose of the study. A randomized trial between SSC and a control group that did not receive SSC was not possible either, because SSC has long been an established practice in our unit. As pointed out, we explored the stress response in mothers and infants in intensive care when exposed to SSC. Thus, we can evaluate the relation among SSC, stress, and intensive care, but we cannot specify the response for specific clinical patient groups. To develop this theme further, it would be of interest to study, for example, different gestational age groups per se. Such studies may render new knowledge that may be of value in guiding which infants would benefit from SSC. One limitation in our study, however, is the relatively small sample size (N = 17), a common problem when studying preterm infants.


   CONCLUSIONS
TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
REFERENCES
 
Mothers express high stress (VAS) before the first SSC, which improves during SSC along with an improved mood. At the fourth SSC, the mother has adapted to the situation and expresses less stress on VAS before the session, and her salivary cortisol and heart rate decrease significant during the SSC. The infants respond to SSC either by increasing or decreasing cortisol concentrations. Infants during SSC have a lower activity level and heart rate and display fewer signs of discomfort and pain. Our results lend support to the use of SSC in the NICU. However, individualized support for the mother at the time of the first SSC and for the preterm infant at every SSC is advisable.


   ACKNOWLEDGMENTS
 
This research was supported by grants from the county and council of Östergötland, Sweden; the Swedish Society of Nursing; the Perinatal Foundation, Linköping; the Sven Jerring Foundation; and the South Sweden Society of Nursing. Special thanks go to our infants and mothers, who made this study possible.


   FOOTNOTES
 
Accepted Jan 25, 2005.

Reprint requests to (E.M.) Department of Molecular and Clinical Medicine, Division of Pediatrics, University Hospital, SE-581 85 Linköping, Sweden. E-mail: evalotte.morelius{at}lio.se

No conflict of interest declared.


   REFERENCES
TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 

  1. Barker DP, Rutter N. Exposure to invasive procedures in neonatal intensive care unit admissions. Arch Dis Child Fetal Neonatal Ed. 1995;72 :F47 –F48[Abstract]
  2. Simons SH, van Dijk M, Anand KS, Roofthooft D, van Lingen RA, Tibboel D. Do we still hurt newborn babies? A prospective study of procedural pain and analgesia in neonates. Arch Pediatr Adolesc Med. 2003;157 :1058 –1064[Abstract/Free Full Text]
  3. Matthews SG, Owen D, Banjanin S, Andrews MH. Glucocorticoids, hypothalamo-pituitary-adrenal (HPA) development, and life after birth. Endocr Res. 2002;28 :709 –718[CrossRef][ISI][Medline]
  4. Grunau RE, Weinberg J, Whitfield MF. Neonatal procedural pain and preterm infants cortisol responses to novelty at 8 months. Pediatrics. 2004;114 (1). Available at: www.pediatrics.org/cgi/content/full/114/1/e77
  5. Abraham E. Effects of stress on cytokine production. Methods Achiev Exp Pathol. 1991;14 :45 –62[Medline]
  6. McEwen BS, Sapolsky RM. Stress and cognitive function. Curr Opin Neurobiol. 1995;5 :205 –216[CrossRef][ISI][Medline]
  7. Sapolsky RM. The possibility of neurotoxicity in the hippocampus in major depression: a primer on neuron death. Biol Psychiatry. 2000;48 :755 –765[CrossRef][ISI][Medline]
  8. Ludington-Hoe SM, Swinth JY. Developmental aspects of kangaroo care. J Obstet Gynecol Neonatal Nurs. 1996;25 :691 –703[CrossRef][Medline]
  9. Bauer K, Uhring 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 –244[CrossRef][ISI][Medline]
  10. Föhe K, Kropf S, Avenarius S. Skin-to-skin contact improves gas exchange in premature infants. J Perinatol. 2000;5 :311 –315
  11. Gale G, Franck L, Lund C. Skin-to-skin (kangaroo) holding of the intubated premature infant. Neonatal Netw. 1993;12 :49 –56[Medline]
  12. Ludington-Hoe SM, Ferreira C, Swinth J, Ceccardi JJ. Safe criteria and procedure for kangaroo care with intubated preterm infants. J Obstet Gynecol Neonatal Nurs. 2003;32 :579 –588[CrossRef][ISI][Medline]
  13. Gray L, Watt L, Blass EM. Skin-to-skin contact is analgesic in healthy newborns. Pediatrics. 2000;105 (1). Available at: www.pediatrics.org/cgi/content/full/105/1/e14
  14. Francis SJ, Walker RF, Riad-Fahmy D, Hughes D, Murphy JF, Gray OP. Assessment of adrenocortical activity in term newborn infants using salivary cortisol determinations. J Pediatr. 1987;111 :129 –133[CrossRef][ISI][Medline]
  15. Magnano CL, Gardner JM, Karmel BZ. Differences in salivary cortisol levels in cocaine-exposed and noncocaine-exposed NICU infants. Dev Psychobiol. 1992;25 :93 –103[CrossRef][ISI][Medline]
  16. Gitau R, Modi N, Gianakoulopoulos X, Bond C, Glover V, Stevenson J. Acute effects of maternal skin-to-skin contact and massage on saliva cortisol in preterm babies. J Reprod Infant Psychol. 2002;20 :83 –88
  17. Davis EP, Townsend EL, Gunnar MR, et al. Effects of prenatal betamethasone exposure on regulation of stress physiology in healthy premature infants. Psychoneuroendocrinology. 2004;29 :1028 –1036[CrossRef][ISI][Medline]
  18. Boyer K, Johnston C, Walker C-D, Filion F, Sherrard A. Does sucrose analgesia promote physiologic stability in preterm neonates? Biol Neonate. 2004;85 :26 –31[CrossRef][ISI][Medline]
  19. Herrington CJ, Olomu IN, Geller SM. Salivary cortisol as indicators of pain in preterm infants. Clin Nurs Res. 2004;13 :53 –68[Abstract]
  20. Mörelius E, Nelson N, Theodorsson E. Salivary cortisol and administration of concentrated oral glucose in newborn infants; improved detection limit and smaller sample volumes without glucose interference. Scand J Clin Lab Invest. 2004;64 :113 –118[CrossRef][ISI][Medline]
  21. Antonini SRR, Jorge SM, Moreira AC. The emergence of salivary cortisol circadian rhythm and its relationship to sleep activity in preterm infants. Clin Endocrinol. 2000;52 :423 –426[Medline]
  22. Huysman MWA, Hokken-Koelega ACS, DeRidder MAJ, Sauer PJJ. Adrenal function in sick very preterm infants. Pediatr Res. 2000;48 :629 –633[ISI][Medline]
  23. Als H, Lawhon G, Brown E, et al. Individualized behavioral and environmental care for the very low birth weight preterm infant at high risk for bronchopulmonary dysplasia: neonatal intensive care unit and developmental outcome. Pediatrics. 1986;78 :1123 –1132[Abstract/Free Full Text]
  24. Stahl F, Amendt P, Dorner G. Total and free cortisol plasma levels in pre- and postnatal life. Endokrinologie. 1979;74 :243 –246[ISI][Medline]
  25. Nelson N, Arbring K, Theodorsson E. Neonatal salivary cortisol in response to heelstick: method modifications enable analysis of low concentrations and small sample volumes. Scand J Clin Lab Invest. 2001;61 :287 –292[CrossRef][ISI][Medline]
  26. Sjöberg L, Svensson E, Persson L. The measurement of mood. Scand J Psychol. 1979;20 :1 –18[ISI][Medline]
  27. Persson LO, Sjöberg L, Svensson E. Mood effects of alcohol. Psychopharmacology (Berl). 1980;68 :295 –299[CrossRef][Medline]
  28. Svensson E, Persson LO, Sjöberg L. Mood effects of diazepam and caffeine. Psychopharmacology (Berl). 1980;67 :73 –80[CrossRef][Medline]
  29. Sandberg M, Wijma K, Wyon Y, Nedstrand E, Hammar M. Effects of electro-acupuncture on psychological distress in postmenopausal women. Complement Ther Med. 2002;10 :161 –169[CrossRef][ISI][Medline]
  30. Luria RE. The validity and reliability of the visual analogue mood scale. J Psychiatr Res. 1975;12 :51 –57[CrossRef][ISI][Medline]
  31. Stevens B, Johnston C, Petryshen P, Taddio A. Premature Infant Pain Profile: development and initial validation. Clin J Pain. 1996;12 :13 –22[CrossRef][ISI][Medline]
  32. Lawrence J, Alcock D, McGrath P, Kay J, MacMurray SB, Dulberg C. The development of a tool to assess neonatal pain. Neonatal Netw. 1993;12 :59 –66[Medline]
  33. Klaus MH, Jerauld R, Kreger NC, McAlpine W, Steffa M, Kennel JH. Maternal attachment. The importance of the first post-partum days. N Engl J Med. 1972;286 :460 –463
  34. Affonso DD, Hurst I, Mayberry LJ, Haller L, Yost K, Lynch ME. Stressors reported by mothers of hospitalized premature infants. Neonatal Netw. 1992;11 :63 –70[Medline]
  35. Folkman S, Lazarus RS. Coping as a mediator of emotion. J Pers Soc Psychol. 1988;54 :466 –475[CrossRef][ISI][Medline]
  36. Smyth J, Ockenfels MC, Porter L, Kirschbaum C, Hellhammer DH, Stone AA. Stressors and mood measured on a momentary basis are associated with salivary cortisol secretion. Psychoneuroendocrinology. 1998;23 :353 –370[CrossRef][ISI][Medline]
  37. Swinth JY, Andersson GC, Hadeed AJ. Kangaroo (skin-to-skin) care with a preterm infant before, during, and after mechanical ventilation. Neonatal Netw. 2003;6 :33 –38
  38. Anderson GC, Moore E, Hepworth J, Bergman N. Early skin-to-skin contact for mothers and their healthy newborn infants [Cochrane Review]. In: The Cochrane Library. Chichester, United Kingdom: John Wiley & Sons, Ltd; 2004
  39. Malone SM, Gunnar MR, Fisch RO. Adrenocortical and behavioral responses to limb restraint in human neonates. Dev Psychobiol. 1985;18 :435 –446[CrossRef][ISI][Medline]
  40. Gunnar MR. Reactivity of the hypothalamic-pituitary-adrenocortical system to stressors in normal infants and children. Pediatrics. 1992;3 :491 –497
  41. Rosenfeld P, Suchecki D, Levine S. Multifactorial regulation of the hypothalamic-pituitary-adrenal axis during development. Neurosci Biobehav Rev. 1992;16 :553 –568[CrossRef][ISI][Medline]
  42. Hanna CE, Keith LD, Colasurdo MA, et al. Hypothalamic pituitary adrenal function in the extremely low birth weight infant. J Clin Endocrinol Metab. 1993;76 :384 –387[Abstract]
  43. Korte C, Styne D, Merritt TA, Mayes D, Wertz D, Helbock HJ. Adrenocortical function in the very low birth weight infant: improved testing sensitivity and association with neonatal outcome. J Pediatr. 1996;128 :257 –263[CrossRef][ISI][Medline]
  44. Acolet D, Modi N, Giannakoulopoulos X, et al. Changes in plasma cortisol and catecholamine concentrations in response to massage in preterm infants. Arch Dis Child. 1993;68 :29 –31[Abstract]
  45. Bond C. Positive touch and massage in the neonatal unit: a British approach. Semin Neonatol. 2002;7 :477 –486[CrossRef][Medline]
  46. Kurihara H, Chiba H, Shimizu Y, et al. Behavioral and adrenocortical responses to stress in neonates and the stabilizing effects of maternal heartbeat in them. Early Hum Dev. 1996;46 :117 –127[CrossRef][ISI][Medline]
  47. Ludington SM. Energy conservation during skin-to-skin contact between premature infants and their mothers. Heart Lung. 1990;19 :445 –451[ISI][Medline]
  48. Ludington-Hoe SM, Hashemi MS, Argote LA, Medellin G, Rey H. Selected physiologic measures and behavior during paternal skin contact with Colombian preterm infants. J Dev Physiol. 1992;18 :223 –232[ISI][Medline]
  49. Gunnar MR, Connors J, Isensee J, Wall L. Adrenocortical activity and behavioral distress in human newborns. Dev Psychobiol. 1988;21 :297 –310[CrossRef][ISI][Medline]
  50. Ferber SG, Makhoul IR. The effect of skin-to-skin contact (kangaroo care) shortly after birth on the neurobehavioral responses of the term newborn: a randomized, controlled trial. Pediatrics. 2004;113 :858 –865[Abstract/Free Full Text]
  51. Vining RF, McGinley RA, Maksvytis JJ, Ho KY. Salivary cortisol: a better measure of adrenal cortical function than serum cortisol. Ann Clin Biochem. 1983;20 :329 –335
  52. Kiess W, Meidert A, Dressendörfer A, et al. Salivary cortisol levels throughout childhood and adolescence: relation with age, pubertal stage, and weight. Pediatr Res. 1995;37 :502 –506[ISI][Medline]
  53. Calixto C, Martinez FE, Jorge SM, Moreira AC, Martinelli CE. Correlation between plasma and salivary cortisol levels in preterm infants. J Pediatr. 2002;140 :116 –118[CrossRef][ISI][Medline]
  54. Schwartz EB, Granger DA, Susman EJ, Gunnar MR, Laird B. Assessing salivary cortisol in studies of child development. Child Dev. 1998;69 :1503 –1513[CrossRef][ISI][Medline]
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International Perspectives: Skin-to-skin Contact: A Paramount Contribution to the Modern Neonatal Paradigm
NeoReviews, February 1, 2007; 8(2): e55 - e57.
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