Infants in the neonatal intensive care unit (NICU) experience stress related to separation from their parents and from painful and noxious procedures.1 These stressors are often necessary or unintended consequences of the care required to keep them alive. Research has shown that infants in the NICU experience, on average, 10 to 14 painful procedures per day.2,3 There is accumulating evidence that chronic stress and repeated painful experiences early in life result in structural and functional changes in the brain as well as reprogramming of the hypothalamic—pituitary–adrenal axis, all of which contribute to lifelong neurodevelopmental and behavioral changes.1,4 Skin-to-skin care (SSC), also known as kangaroo care, is an intervention commonly used in the NICU where the infant is held by a parent or caregiver with direct skin-on-skin contact. SSC has been shown to have a variety of benefits to the infant and parents, including improved breastfeeding, growth, neurodevelopment, parent–infant attachment, parent stress, and reduced infections.5–9 SSC is also frequently considered a stress-reducing intervention for infants in the NICU. The purpose of this systematic review was to answer the following clinical question: In premature infants in the NICU, what is the available evidence that SSC improves short-term physiologic stress outcomes compared with incubator care?
SELECTION OF RELEVANT OUTCOME MEASURES
In this systematic review, we were interested in evaluating the evidence related to changes in stress resulting from SSC. Physiologically, neonates respond to stress in multiple ways. During times of reduced stress, the parasympathetic nervous system is activated, resulting in improved ability to engage with caregivers, conservation of energy for growth and development through lower heart rate and respiratory rates, increased heart rate variability, and release of oxytocin.10,11 Heart rate variability is the variation in time between heart beats and is a measure of balance between sympathetic (suggesting more stress) and parasympathetic (suggested less stress) activity.10 Oxytocin is a hormone most often associated with its role in labor and delivery, but also plays a critical role in bonding and attachment; oxytocin increases during times of relaxation, stress reduction, and bonding.11
When neonates experience heightened stress, they first respond with activation of the sympathetic nervous system (ie, increased heart rate, increased respiratory rate, and decreased heart rate variability) and activation of the hypothalamic—pituitary–adrenal axis (ie, increased release of cortisol).12 Cortisol is a glucocorticoid hormone released in response to hypothalamic—pituitary–adrenal axis activation during stress and can be measured in the blood, saliva, or urine as a short-term measure of stress.12 If the infant cannot manage the level of stress with this initial reaction, the secondary stress response via the unmyelinated portion of the vagus results in apnea and bradycardia.13,14 Apneic events can result in a drop in oxygen saturation of the blood. Based on the physiologic responses to stress, the following outcome measures were determined to be relevant to this systematic review: heart rate (HR), respiratory rate (RR), oxygen saturation (SpO2), heart rate variability (HRV), apnea, bradycardia, oxytocin, and cortisol.
PubMed and CINAHL were each searched in September 2018 using the following terms: ((skin-to-skin) or (skin to skin) or (kangaroo care) or (kangaroo mother care)) and ((stress) or (sympathetic nervous system) or (autonomic nervous) or (heart rate variability) or (physiolog*)) and ((preterm) or (premature)). The following limits were placed on the search: full text, English language, and journal article (in PubMed) or research article (in CINAHL). No limits were placed on the time of publication.
Articles identified through this search were screened by title and abstract to determine whether they met inclusion criteria. To be included in this systematic review, the article had to (1) report on an original research study in which SSC was compared with incubator care in premature infants in the NICU and (2) report one of the relevant stress-related neonatal outcome measures described previously. Articles that clearly did not meet inclusion criteria based on the abstract and title screening were excluded. The remaining articles were reviewed in full text to confirm inclusion and exclusion criteria were met.
During full-text review, articles were excluded if they did not report the results of an original research study (ie, review article), the study did not measure infant stress outcomes during SSC compared with incubator care (ie, only measured parent stress outcomes or only measured outcomes before and after SSC, not during), the study was conducted outside the NICU, or if a full-text version of the article could not be obtained (eg, an unpublished dissertation). In addition, articles were excluded if they were published prior to the year 2000 because the use of postnatal corticosteroids was common during this time, which may have effects on the stress response. Finally, articles that reported on the effect of SSC as an intervention during a painful or stressful procedure were excluded. A 2017 Cochrane review on SSC for procedural pain in neonates systematically reviewed this literature and concluded that SSC is an effective intervention to reduce pain associated with a single painful procedure.15 The systematic review presented in this article aimed to review the current available evidence on the effects of SSC on short-term physiologic stress outcomes separate from painful procedures. The reference lists of articles meeting inclusion and exclusion criteria were then reviewed to identify additional literature for screening.
The results of the search strategy and identification of literature for inclusion in the systematic review are provided in Figure 1. The search identified 1280 unique articles, of which 72 were identified as being relevant to this review and assessed for eligibility. After removing articles that did not meet inclusion/exclusion criteria, 19 articles were included in this systematic review (Table 1). These 19 articles are discussed based on their outcome measures in the following categories: cardiorespiratory outcomes of SSC and cortisol and oxytocin outcomes of SSC.
Cardiorespiratory Outcomes of SSC
There are currently 15 articles that report on short-term cardiorespiratory outcomes during SSC in preterm infants compared with incubator care in the NICU. The results have been mixed, with some studies finding changes in cardiorespiratory parameters that would indicate reduced physiologic stress (ie, decreased HR, RR, apnea and bradycardia, and increased SpO2 and HRV), while other studies have reported changes in cardiorespiratory parameters that would indicate increased physiologic stress during SSC compared with incubator care. More studies have reported positive effects of SSC on cardiorespiratory parameters than negative effects, but the majority of studies have reported no statistically significant differences.
Thirteen studies reported on heart rate outcomes during SSC compared with incubator care; 12 reported raw values of HR, which are presented in Figure 2. Carbasse and colleagues16 did not report raw values for HR, so this study is not included in Figure 2, but they reported that HR decreased by 3.5 beats/min during SSC compared with incubator care (P = .001). Of the 13 studies reporting HR, only 6 studies found statistically significant differences between SSC and incubator care. Four studies found that HR decreased significantly during SSC,16–19 while 2 studies found that HR increased significantly during SSC.20,21 The remaining 7 studies found no statistically significant differences in HR between SSC and incubator care.22–28
Ten studies reported on RR outcomes during SSC compared with incubator care; 9 of these studies reported raw values of RR, which are presented in Figure 3. Carbasse and colleagues16 did not report raw values for RR, so their results are not included in Figure 3, but they found no significant difference in RR between SSC and incubator care (P = .13). Of the 10 studies reporting RR outcomes, only 5 found statistically significant differences. Three studies found that RR was significantly lower during SSC,17–19 while 2 studies found that RR was significantly higher during SSC.20,22 The remaining 5 studies did not find a statistically significant difference in RR between SSC and incubator care.16,23,25,27,28
Ten studies reported on SpO2 as a short-term outcome of SSC; 8 of these studies reported raw values for SpO2, which are shown in Figure 4. Carbasse et al16 and Buil et al17 did not report raw values and are not included in Figure 4. Carbasse and colleagues16 reported that SpO2 increased by 1.5% during SSC compared with incubator care (P = .005). Buil and colleagues17 found no statistically significant difference between SSC and incubator care for SpO2. Of the 10 studies reporting SpO2 findings, only 3 studies found statistically significant differences between SSC and incubator care. Carbasse et al16 found a significant increase in SpO2 during SSC, while Lorenz et al26 found a statistically significant decrease in SpO2 during SSC (93.6% in SSC vs 94.1% in incubator; P < .05), although this 0.5% difference is not likely to be clinically significant. One study by Lorenz et al21 reported median SpO2 as the same between SSC and incubator care (97% vs 97%), but the findings were statistically significant (P = .02) because the interquartile range for the SSC was lower than incubator care; this does not reflect a clinically significant difference. The remaining 7 studies did not find a statistically significant difference in SpO2 between SSC and incubator care.17,19,20,22,23,25,27 Mitchell and colleagues29 did not report SpO2, but reported on desaturation events and found that infants had fewer desaturation events during SSC than in the incubator (P < .05).
Heart Rate Variability
Five studies have reported outcome measures related to HRV during SSC compared with incubator care. Three of these studies were by the same author and reported on the same time domain and frequency domain measures of HRV,18,19,30 but Bloch-Salisbury et al23 and Butruille et al24 each reported on different HRV outcome measures. Bloch-Salisbury et al23 reported no significant differences in heart rate variance between SSC and incubator care. Butruille et al24 reported HRV using the Newborn Infant Parasympathetic Evaluation (NIPE) and found no difference in NIPE scores between SSC and incubator care for the sample as a whole, but found that infants responded differentially based on baseline parasympathetic activity. Infants with lower parasympathetic activity prior to SSC responded with an increase in NIPE during SSC (P < .05), while those with higher parasympathetic activity at baseline did not respond significantly. In other words, infants who were more stressed during incubator care responded positively (ie, reduced stress) during SSC, but infants who were less stressed during incubator care did not show a significant change in stress during SSC.
In the series of studies recently published by Kommers et al,19 they reported no statistically significant HRV findings in 1 study and significantly lower HRV across almost all measures of HRV during SSC compared with incubator care in the other 2 studies.18,30 The vast majority of work using HRV has been conducted in adults and the current interpretation of HRV parameters is based on adult physiology. Kommers and colleagues18 have challenged the interpretation of these HRV parameters for neonates, pointing to key differences in neonatal physiology, specifically that certain parasympathetic branches of the nervous system may not be fully developed in preterm infants and infants are more likely to experience decelerations in HR. Kommers et al18 suggest that their findings that HRV parameters decreased during SSC compared with incubator care should be interpreted as a positive effect of SSC and an indication of greater stability in response to parental coregulation.
Four studies reported on episodes of apnea during SSC compared with incubator care and none found a statistically significant difference in frequency of apneic events.20,25,27,28
Five studies reported bradycardia as a physiologic outcome during SSC compared with incubator care. Four of these studies found no difference in number of bradycardic events between SSC and incubator care.17,20,21,25 Mitchell et al, 29 however, found that infants had fewer bradycardic events while being held in SSC compared with when the infant was in the incubator (P < .05).
Cortisol and Oxytocin Outcomes of SSC
Three studies have evaluated infant cortisol response to SSC31–33 while 2 studies have evaluated the oxytocin response to SSC.33,34 The results of these studies have supported SSC as a stress-reducing intervention compared with incubator care.
Mirnia and colleagues31 found no statistically significant difference in salivary cortisol levels between infants receiving 45 minutes of SSC with their fathers and infants receiving incubator care. The other 2 studies reporting cortisol as a physiologic outcome of SSC did find statistically significant differences between SSC and incubator care. Neu and colleagues32 found that infant salivary cortisol levels decreased during a 1-hour SSC session compared with prior to SSC (P < .01). Similarly, Vittner and colleagues33 found that salivary cortisol decreased during a 60-minute SSC session compared with baseline; this finding was consistent whether SSC was provided by the mother or the father (P < .001).
Vittner and colleagues33 found that salivary oxytocin levels increased significantly during 1 hour of SSC compared with measurements taken prior to SSC (P = .002). Kommers and colleagues34 found that oxytocin responses to SSC differed by comfort scores at baseline. While they report that, overall, oxytocin decreased during SSC compared with incubator care (P = .03), they report that infants who were more comfortable at baseline had a positive oxytocin response to SSC while infants who were more uncomfortable at baseline had a drop in oxytocin levels during SSC.
Strengths and Weaknesses of the Currently Available Evidence
Overall, there is more evidence to support that SSC has positive effects on short-term physiologic stress outcomes when compared with incubator care than negative effects. The mixed findings for some cardiorespiratory outcomes likely reflect differences in the study procedures (eg, duration of SSC), data collection, and data analysis. In addition, many of the studies included in this review did not find statistically significant differences in stress outcomes. The reason for this lack of statistical significance likely has to do with the small sample sizes included in most of the studies and differences in study procedures, inclusion and exclusion criteria, data collection, and analyses.
Variations in Sample, Inclusion, and Exclusion Criteria
There is significant variability among studies in terms of the samples studied and the exclusion criteria used. Many of the studies excluded the most vulnerable infants (Table 1), likely because of safety concerns, but these are the infants who may benefit most from an SSC intervention. The wide variation in gestational ages included and the infant's age at the time of study make it difficult to compare study results and limit the generalizability of the findings. The lack of statistically significant findings in many of the studies presented in this review was likely due to inadequate sample sizes. Most studies did report power analyses to support whether the sample size was adequate to find statistical significance.
Variations in SSC Procedures
There is significant variation in how SSC is practiced and how it is carried out as part of a research study. In the studies presented in this review, the duration of SSC ranged from 45 minutes to 6.5 hours, and frequency ranged widely as well (Table 1). The conditions of SSC were also very different between studies. While some studies provided very clear details about how SSC was conducted (eg, positioning of the infant and degree of recline of the parent) and ways in which the environment was altered (eg, noise limited and temperature maintained), other studies did not account for these other variables or did not describe the intervention in enough detail for the methods to be recreated in future studies. The timing of tube feedings and any stressful events (eg, blood draw) in relation to the SSC session were also frequently not described.
Variations in Control Conditions
There were also inconsistencies across studies in terms of the conditions of incubator care. There were some studies that did an excellent job of controlling the condition of incubator care, specifically the infant's position, timing around feeding, and timing around other care. In studies where an SSC intervention was compared with an incubator care group, some studies controlled the amount of holding or SSC in the incubator care group, while other studies did not state whether any of these factors were taken into consideration.
Controlling for Diurnal Changes in Outcomes
Some of the short-term physiologic stress outcomes included in this review are affected by diurnal changes, specifically HRV, oxytocin, and cortisol. A significant strength of the study by Vittner and colleagues33 was that they controlled for these diurnal changes by collecting salivary samples with a 2-hour period of the day. The stress response system is a highly complex system and taking into account as many of these factors as possible improves the likelihood that findings are truly due to skin-to-skin contact and not time of day, position, or other interfering factors.
Statistical Analyses of Physiologic Data
There are a variety of ways in which physiologic data can be collected and analyzed. While some studies report periodically recording values (eg, every 5 minutes HR is recorded), other studies report continuously measuring cardiorespiratory parameters. Continuous measurement of physiologic data allows for more rich and accurate data, particularly in the preterm population where there tends to be significant minute-to-minute variation in physiologic parameters. In addition, there are different ways in which repeated physiologic measurements can be analyzed, with some of the more advanced techniques allowing for optimization of the power of these data. When continuous physiologic data are collected, linear mixed modeling is an advanced statistical technique that allows for longitudinal measurements of physiology (eg, every 1 minute for 2 hours). Linear mixed modeling optimizes power by using many repeated measurements while taking into account correlation with baseline values, correlation between measurements within the same infant, and change over time with increasing SSC duration. A thorough overview of linear mixed modeling is outside of the scope of this article, but examples of studies using this technique for the analysis of physiologic data are provided here for those interested.35,36 Using advanced statistical methods in future studies could allow for better comparison of the physiologic changes in response to SSC.
Recommendations for Practice
Although there are some mixed findings, there are more studies that support SSC as having stress-reducing effects on physiologic stress outcomes compared with incubator care. Many studies did not find statistically significant differences in physiologic variables, which is likely a result of sample size and controlling for other factors, as described previously. There is very little data to suggest that SSC has negative effects on stress in infants, even very fragile infants. There are understandably barriers to providing SSC in the NICU, but neonatal nurses are in the unique position to facilitate SSC and it is likely that earlier, more frequent, and longer durations are going to have the most stress-reducing benefits, especially for the most vulnerable infants.37 There is also evidence that infants benefit similarly from SSC provided by fathers.38 Neonatal nurses can encourage other caregivers (eg, fathers, grandparents, and siblings) to become involved as well. Given the positive effects of SSC on infant stress as described in this article as well as positive effects on pain responses,15 breastfeeding outcomes,6 maternal stress,5 parent–child interaction, and infant growth and development,39,40 SSC should be considered an essential component of providing optimal NICU care.
Recommendations for Research
No clear data exist on the ideal timing of initiation of SSC, the duration of SSC on a given day, or the frequency of SSC to optimize the stress-reducing effects of SSC. Future research on SSC in infants in the NICU should ensure adequate sample sizes for statistical power, utilize sophisticated data collection and analysis strategies to optimize the quality of the data, and carefully consider the study design (eg, the amount of SSC allowed in the usual care comparison group) and confounding factors (eg, number of stressful procedures) during study planning, conduction, and data analysis. SSC is likely to have the greatest impact on the most vulnerable infants in the NICU, who are likely to endure the most painful and stressful procedures and be at the highest risk for interruption of parent–child bonding. Kommers et al34 and Butruille et al24 both found that infants responded differentially to SSC based on their baseline level of comfort and stress level. Future studies should explore these factors and consider that SSC may be more beneficial to certain populations than others. In the studies included in this review, infants with intraventricular hemorrhage grade 3 or more, congenital anomalies, chromosomal disorders, and surgical procedures were frequently excluded from participating in the research. Future research needs to include these infants to explore the safety, risks, and benefits of SSC in stable preterm infants as well as infants with medical complexity.
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