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Skin-to-skin care for procedural pain in neonates

  1. Celeste Johnston1,*,
  2. Marsha Campbell-Yeo2,
  3. Ananda Fernandes3,
  4. Darlene Inglis2,
  5. David Streiner4,
  6. Rebekah Zee2

Editorial Group: Cochrane Neonatal Group

Published Online: 23 JAN 2014

Assessed as up-to-date: 16 MAY 2013

DOI: 10.1002/14651858.CD008435.pub2


How to Cite

Johnston C, Campbell-Yeo M, Fernandes A, Inglis D, Streiner D, Zee R. Skin-to-skin care for procedural pain in neonates. Cochrane Database of Systematic Reviews 2014, Issue 1. Art. No.: CD008435. DOI: 10.1002/14651858.CD008435.pub2.

Author Information

  1. 1

    McGill University, Ingram School of Nursing, Quebec, Canada

  2. 2

    IWK Health Centre, Neonatal Intensive Care Unit, Halifax, Nova Scotia, Canada

  3. 3

    Coimbra College of Nursing, Department of Child Health, Coimbra, Portugal

  4. 4

    Department of Clinical Epidemiology and Biostatistics, Room 3G31, Kunin-Lunenfeld Applied Research Unit, North York, Ontario, Canada

*Celeste Johnston, Ingram School of Nursing, McGill University, Quebec, H3A 2T5, Canada. celeste.johnston@mcgill.ca.

Publication History

  1. Publication Status: New
  2. Published Online: 23 JAN 2014

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Background

  1. Top of page
  2. Background
  3. Objectives
  4. Methods
  5. Results
  6. Discussion
  7. Authors' conclusions
  8. Acknowledgements
  9. Data and analyses
  10. Contributions of authors
  11. Declarations of interest
  12. Sources of support
  13. Index terms
 

Description of the condition

The preterm neonate frequently spends the first days or weeks of life in the Neonatal Intensive Care Unit (NICU), where numerous noxious procedures are part of routine care (Johnston 1997; Simons 2003; Stevens 2003; Johnston 2008; Johnston 2011b). There is substantial evidence that long-term blunting of behavioural, autonomic, and hormonal responses to pain is a result of early untreated exposure to pain in preterm neonates (Johnston 1996; Oberlander 2000; Grunau 2007a; Grunau 2007b). The most common painful procedures are heel lance and intravenous line insertions. Topical anaesthetics have not been found to be effective in this population (Larsson 1996; Stevens 1999). Sucrose has been shown to be effective (Stevens 2010a) but frequently repeated doses of sucrose in the very preterm neonate may not be safe (Johnston 2002; Lefrak 2006; Johnston 2007a). Parenteral analgesics either have negative sequelae (Marsh 1997; Anand 2004; Carbajal 2005) or have not been tested for pain in this population (Cuzzolin 2001). Behavioural methods of pain control such as non-nutritive sucking, simulated rocking, facilitated tucking and positioning have been tested, with non-nutritive sucking having a significant effect even in very preterm neonates (Campos 1994; Corff 1995; Stevens 1999a; Akman 2002; Carbajal 2002; Boyle 2004; Cignacco 2007). There is a large volume of literature on pain in neonates, including a review of over 40 measures of pain (Stevens 2007). Several studies have reported important age differences in response, with more preterm neonates having less robust and sustained responses (Craig 1984; Johnston 1993; Stevens 2007; Gibbins 2008).

 

Description of the intervention

Recently there has been growing interest in how mothers of preterm neonates can contribute to the promotion of growth and comfort in the NICU setting. This has been based on two premises: (1) the loss of comfort-providing roles of parents in critical care settings, and (2) the effect of maternal touch specifically in the skin-to-skin care (SSC) paradigm, or Kangaroo Care (KC), on various parameters of neonatal stability and state regulation. In studies of parents of critically ill children and infants, parents were concerned about pain management and found their child’s suffering a primary source of stress (Miles 1992; Youngblut 1992; Moehn 1996; Wereszczak 1997). Even in situations where the staff believed that they were handling the child’s pain well and that the parents were not distressed, this was not the case from the parents’ perspective (Simons 2001). In a US and UK study of 11 NICUs, with 200 parents, almost all parents reported that their infant had experienced moderate to severe pain that was worse than they had expected (Franck 2001). Concerns about pain predicted the most important variance of parental stress. Another major concern of parents is the loss of their parental role, including to provide comfort (Miles 1989; Shields-Poe 1997; Ko 1998). In the above study of NICU parents (Franck 2002), 87% stated that they would wish to participate in managing their infant’s pain. In a study of mothers engaged in KC while their infants underwent routine heel lance in the NICU, 80% of the mothers reported positive feelings and 90% said they would do it again (Campbell-Yeo 2008).

SSC, referred to as KC because of its similarity to marsupial behaviour, was first developed as a method of providing warmth for low birth weight infants in Bogota, Columbia in 1979 (Whitelaw 1985). During SSC, a diaper-clad infant is held upright between the mother's breasts, at an angle of approximately 60 o, providing maximal skin-to-skin contact between the baby and parent. A survey on the holding policy in 215 NICUs in the US indicated that almost three-quarters of the units allowed parents to hold their extubated infant in SSC (Franck 2002). There is extensive literature on KC in developing countries that is not reviewed here (Charpak 2005).

 

How the intervention might work

An updated review of clinical trials of SSC on targeted infant outcomes of breastfeeding, behaviour, and physiological adaption in healthy neonates found 30 studies that met the inclusion criteria, four being with late preterm infants (Moore 2007). They reported evidence supporting SSC for success and duration of breastfeeding (Carfoot 2003; Johnson 2006; Moore 2007). Physiological stability and temperature control have been consistently reported as improved during SSC (deLeeuw 1991; Christensson 1992; Bauer 1998; Ludington-Hoe 1999; Gazzolo 2000; Bohnhorst 2001; Chwo 2002; Ibe 2004; Ludington-Hoe 2004; McCain 2005; Hunt 2008). For a newborn, behaviour is primarily based on the sleep and wake state dimension of neurobehavioural organization involving the ability to make smooth transitions between sleep, quiet, and awake phases; and to maintain the most desirable state of quiet sleep (Ludington-Hoe 1996). Several studies have shown that one to three hours spent in SSC resulted in increased frequency of quiet sleep, longer duration of quiet sleep, and decreased crying (deLeeuw 1991; Ludington-Hoe 1992; Michelsson 1996; Feldman 2002; Erlandsson 2007; Kostandy 2008). For example, a randomised controlled trial (RCT) of healthy newborns randomly assigned to receive KC for one hour starting within 15 minutes after birth found that at the four hour observation time KC infants slept longer, were mostly in a quiet sleep state, exhibited more flexor movements and postures, and showed fewer extensor movements (Ferber 2004). Feldman and colleagues have reported sustained neurobehavioural regulation from 30 to 37 weeks gestational age as a result of early KC in the NICU (Feldman 2003). A Cochrane review by Conde-Agudelo reported three studies on mortality and morbidity and did not address pain response (Conde-Agudelo 2003). Given that SSC promotes autonomic stability and state regulation as well as bonding between the mother and the infant, it is logical that it would be tested as an intervention for pain where the response to noxious stimuli includes autonomic arousal and crying, in addition to giving mothers back their comforting role.

 

Why it is important to do this review

The American Pediatric Society and Canadian Paediatric Society Committees on Fetus and Newborn incorporated SSC as a recommended intervention. However, no systematic review with the rigour of The Cochrane Collaboration has been conducted. There could, for example, be a publication bias that would favour positive outcomes. There has been a Cochrane review of SSC for mortality and morbidity (Conde-Agudelo 2003), which did favour SSC over usual care controls for infections and weight gain.

 

Objectives

  1. Top of page
  2. Background
  3. Objectives
  4. Methods
  5. Results
  6. Discussion
  7. Authors' conclusions
  8. Acknowledgements
  9. Data and analyses
  10. Contributions of authors
  11. Declarations of interest
  12. Sources of support
  13. Index terms
 

Primary objectives

  1. To determine the effect of SSC alone on pain from medical or nursing procedures in neonates undergoing painful procedures compared to no intervention, sucrose or other analgesics, or additions to simple SSC such as rocking.
  2. To determine the effects of the amount of SSC (duration in minutes), method of administration (who provided the SSC, positioning of caregiver and neonate pair) of SSC in reducing pain from medical or nursing procedures in neonates.

 

Secondary objectives

  1. To determine the safety of SSC care for relieving procedural pain in infants, specifically reports of:
    1. bradycardia (heart rate less than 100 for 15 seconds),
    2. desaturation (transcutaneous oxygen saturation readings of less than 80% for 15 seconds), or
    3. apnoea (absence of spontaneous respiration for 20 seconds, or 10 seconds if accompanied by bradycardia or desaturation (Lagercrantz 1992)).
  2. To compare the outcomes of neonates receiving SSC in the following postmenstrual age categories: less than 32 weeks, 32 to 36 weeks, full term (37 to 42 weeks).

 

Methods

  1. Top of page
  2. Background
  3. Objectives
  4. Methods
  5. Results
  6. Discussion
  7. Authors' conclusions
  8. Acknowledgements
  9. Data and analyses
  10. Contributions of authors
  11. Declarations of interest
  12. Sources of support
  13. Index terms
 

Criteria for considering studies for this review

 

Types of studies

Studies with randomisation or quasi-randomisation, and blinded (for example, coding video tapes of infant faces only or using physiological data from monitors) or not blinded assessors for pain response were considered for inclusion. This included different designs such as classic randomised controlled trials, randomised cross-over trials, and cluster as well as quasi-experimental designs.

 

Types of participants

Term infants (> 37 completed weeks postmenstrual age (PMA)) and preterm infants (< 37 completed weeks PMA) to a maximum of 44 weeks PMA receiving SSC for painful procedures conducted by doctors, nurses, or other healthcare professionals. The painful procedures that were included are those that are tissue damaging or considered painful, such as endotracheal suctioning (Carbajal 2008).

 

Types of interventions

The infant, wearing no more than a diaper, in ventral skin contact with another person during a painful procedure. We were interested in any comparisons of dosage (duration of time in SSC), any adjuvant therapies (sucrose or other sweet tastes, pacifier, topical anaesthetics, systemic analgesics), provider of SSC (mother, father, nurse, other), and variations of SSC such as the addition of rocking or music.

 

Types of outcome measures

 

Primary outcomes

Pain response to or recovery from an invasive procedure, or both, as measured by at least one of the following.

  1. Behavioural indicators (audible cry duration in seconds or milliseconds; proportion of time of total procedure time audible crying; proportion of time of total procedure that had predefined facial actions reflecting grimace e.g., brow bulge, eye squeeze, nasolabial furrow; proportion of time that had predefined body movements e.g., limb thrashing, fisting, finger splaying, limb and torso flexion).
  2. Physiological indicator changes from baseline or between groups in heart rate (HR), respiratory rate, oxygen (O2) saturation/transcutaneous oxygen tension (tcpO2), and near-infrared spectroscopy (NIRS). These measures should be reported before the tissue damaging part of the procedure, during the procedure, and in the time to recovery following the procedure.
  3. Hormonal indicators (salivary cortisol, serum beta-endorphins) obtained from body fluids (saliva, serum) with description of analyses e.g., radio-immune assay techniques.
  4. Validated composite pain scores (including a combination of behavioural, physiological, and contextual indicators). There are over 50 measures of pain in neonates in the literature. The ones that we assessed as being valid for neonates undergoing procedural pain include:
    1. Premature Infant Pain Profile (PIPP) (Stevens 1996; Stevens 2010b). The PIPP includes gestational age, behavioural state, heart rate, oxygen saturation, and three facial reactions (brow bulge, eye squeeze, and nasolabial furrow). The range is 0 to 21 with a score of 6 indicating pain.
    2. COMFORT scale (van Dijk 2000). This scale measures alertness, calmness, respiratory response or crying, physical movement, muscle tone and facial tension, and separate latent variables for heart rate (HR) baseline and mean arterial blood pressure baseline (MAP).
    3. Behavioral Indicators of Infant Pain (BIIP) (Holsti 2007). The BIIP combines sleep and wake states, five facial actions and two hand actions.
    4. Neonatal Infant Pain Scale (NIPS) (Lawrence 1993). The NIPS includes facial expression, cry, breathing pattern, arms, legs, state of arousal.
    5. Neonatal Pain, Agitation, and Sedation Scale (N-PASS) (Hummel 2008; Hummel 2010). N-PASS was originally developed to measure ongoing pain but has recently been validated as a measure of acute pain. It includes crying and irritability, behaviour and state, facial expression, extremities and tone, and vital signs (heart rate, respiratory rate, blood pressure, oxygen saturation). It also has scores that rate sedation as well as pain and agitation.

All of these indicators yield continuous data.

There are repeated measures across time and conditions within participants. For the cross-over design studies, the first condition was analysed.

These indicators were taken immediately prior to, during, and immediately following the painful procedure. The differences between the changes from baseline between groups were used.

 

Secondary outcomes

Response of SSC provider, including self-report, cortisol, and physiological indicators. 

Adverse events including (Lagercrantz 1992):

  1. bradycardia (heart rate less than 100 for 15 seconds),
  2. desaturation (transcutaneous oxygen saturation levels less than 80 for 15 seconds),
  3. apnoea (absence of spontaneous respirations for more than 20 seconds or for 10 seconds if accompanied by bradycardia or desaturation).

These indicators are binary and were categorized as yes or no.

 

Search methods for identification of studies

 

Electronic searches

We performed electronic searches using the following sources: Cochrane Central Register of Controlled Trials (CENTRAL) in The Cochrane Library; Evidence-Based Medicine Reviews; MEDLINE (1950 to January 2013); PubMed (1975 to January 2013); EMBASE (1974 to January 2013); CINAHL (1982 to January 2013); Web of Science (1980 to January 2013); LILACS database (1982 to January 2013); SCIELO database (1982 to January 2013); PsycInfo (1980 to January 2013); AMED; Dissertation-Abstracts International (1980 to January 2013). The limits were humans, but with no language limits.

The types of articles were: clinical trial, meta-analysis, RCT, review.

Duplicates were excluded.

Key words and MeSH terms included: infant/newborn OR premature OR low birth weight AND painful procedure OR invasive procedure OR heel lance OR heel stick OR blood procurement OR venipuncture OR intravenous start OR arterial line insertion OR injection OR immunization AND analgesia OR pain OR comfort AND skin-to-skin OR kangaroo care OR kangaroo mother care AND randomised controlled trial OR controlled clinical trial OR crossover design OR random allocation OR blinding.

 

Searching other resources

In addition to the electronic searches noted above, we searched the following sources: Canadian Agency for Drugs and Technologies in Health (CADTH), University of British Columbia (UBC) Library, EAGLE, National Technical Information Service (NTIS), PsycEXTRA, Wikipedia, Web of Knowledge. We manually searched bibliographies of the most recent relevant paediatric, neonatal, and pain journals and recent major paediatric pain conference proceedings. We did not include unpublished studies. We listed abstracts under excluded studies. We did not impose language restrictions.

We made efforts to seek unpublished studies using Paediatric Pain and Neonatology Listservs requesting readers to reply.

 

Data collection and analysis

We developed a data extraction Excel file that allowed decisions to be made about whether or not to include a study for initial selection. We selected studies that addressed the efficacy and safety of SSC compared to another condition for relieving pain in infants. Four review authors (MCY, AF, DI, RZ) independently screened the titles and abstracts of all the references retrieved by the search strategy. At this stage, efforts were made to aim more for sensitivity than specificity, that is, we wished to be more inclusive than exclusive.

We resolved any differences by discussion among the screening review authors as well as a fifth review author (CJ). We used RevMan 5 software to collate the data.

 

Selection of studies

Using the studies selected from the above steps, we independently assessed the full texts of relevant papers to determine whether or not they met the inclusion criteria. We evaluated studies for methodological quality and appropriateness for inclusion according to the selection criteria. We resolved disagreements by discussion with two review authors (CJ and DS). DS verified the decisions.

We used the electronic form regarding 'Risk of bias' and 'Table 8.5a' from the Cochrane Handbook for Sysyematic Reviews of Interventions.

We listed rejected studies in the 'Characteristics of excluded studies' table, and we recorded the reasons for exclusion. Review authors were not blinded to author, institution, journal, or results of a study for its assessment.

All studies meeting the inclusion criteria underwent quality assessment and data extraction.

 

Data extraction and management

The following data were extracted.

  • Study designs: methods of randomisation, intervention, cross-over design, single centre or multi-centric.
  • Participants: PMA, sex, postnatal age at time of intervention, setting.
  • Interventions: position duration, provider, adjuvant therapies (pharmacologic and non-pharmacologic).
  • Outcomes: pain indicator (behavioural, physiological, and composite), recovery times.
  • Side effects, provider response, study refusals, withdrawals and dropouts, if reported.

We made attempts to contact the study authors if data were missing or needed to be clarified.

 

Assessment of risk of bias in included studies

We used the guidance from the Cochrane Handbook for Systematic Reviews of Interventions (Table 8.5a) and the electronic form regarding 'Risk of bias'. We examined:

  1. sequence generation;
  2. allocation concealment;
  3. blinding of participants, personnel, assessors;
  4. incomplete outcome data;
  5. selective outcome reporting;
  6. other possible sources of bias.

There were three possible answers: low risk, high risk, and unclear risk.

Funnel plots were not performed given the small number of papers that could be combined for analysis.

Four review authors (MCY, AF,CJ, RZ) independently scored each study for quality, with verification by a methods expert (DS).

 

Measures of treatment effect

In studies with continuous data, mean differences (MD) and standard deviations (SD) in each group and effect size (ES) for the total were used.

 

Unit of analysis issues

The unit of analysis was the neonates receiving SSC. There were instances in which there were repeated measures, for example, scores taken every 30 seconds within a condition (SSC or comparison). There were no cluster randomised trials.

For cross-over trials, the first condition data were used and the study was treated as an RCT (Elbourne 2002).

 

Dealing with missing data

We contacted all authors of studies for missing data, or if clarification was required. When the contact was not reciprocated, or the author was unable to provide the requested data, the study was excluded from the data synthesis.

 

Assessment of heterogeneity

The decision to perform a meta-analysis was based on the clinical decision regarding the appropriateness of combining trials and outcomes. Heterogeneity was explored using the I2 statistic. Given the variability in the type of intervention, outcomes measured, etc., it was safe to assume that we were not estimating a single effect size but rather a distribution of effect sizes. Consequently, we used a fixed-effect model (Erez 1996; Hedges 1998; Overton 1998; Field 2003).

The statistical analysis was performed using RevMan 5.1 software, which is provided by The Cochrane Collaboration. We applied the Chi2 test (Q test) and the I2 statistic to assess between-study heterogeneity. With continuous data, we expressed the effect as weighted mean difference (WMD) and 95% confidence interval (CI).

 

Assessment of reporting biases

We sought protocols in trial registries and compared the reports to the protocols in order to determine if there might be selective reporting. We would have attempted to contact the corresponding authors if there had been discrepancies, but there were none.

In examining the studies for duplication bias, we closely examined articles from repeated authors or sites and compared sample size, characteristic, and details of the studies. When there appeared to be overlap, we attempted to contact the corresponding author, or when everything was similar we assumed it was a duplicate and included only one of the articles.

When we were not successful in contacting authors, the possible sources of reporting bias were included in our conclusions.

We had planned to do an analysis of publication bias to determine if negative results were less likely to be published in peer-reviewed journals. However, we found no examples of significant negative results, other than for one of several outcomes in one study, including in trial registries and in the grey literature. Therefore, this analysis was not conducted.

We examined the range of languages, locations, and citation sources to examine potential bias. Only English language reports were found, although some were from non-anglophone countries.

 

Data synthesis

For studies using similar outcomes, both in terms of the pain indicator and the time frame examined, data were congregated and analysed together. We computed mean differences and standardized mean differences (log transformations). Data were entered into RevMan via the table of means and standard deviations per group in order to develop a forest plot.

 

Subgroup analysis and investigation of heterogeneity

We were unable to form group analyses as we had intended for the following categories: gestational age less than 32 weeks, between 32 to 36 weeks, and full term (37 to 42 weeks); or duration or 'dose' of SSC. There were not sufficient studies with similar outcomes to compare the effect of SSC on these factors.

As above, we performed heterogeneity tests using the Chi2 test and I2 statistic.

 

Sensitivity analysis

We were not able to conduct a sensitivity analysis as there were not enough studies examining similar outcomes with similar age groups or procedures.

 

Results

  1. Top of page
  2. Background
  3. Objectives
  4. Methods
  5. Results
  6. Discussion
  7. Authors' conclusions
  8. Acknowledgements
  9. Data and analyses
  10. Contributions of authors
  11. Declarations of interest
  12. Sources of support
  13. Index terms
 

Description of studies

See Characteristics of included studies and Characteristics of excluded studies below.

 

Results of the search

A total of 39 studies were identified for possible inclusion in this first review. An additional study (the 38th) was found as an abstract, but had not been published at the time of review preparation. Of the 39 studies, 19 were included. Two reports (Sajedi 2007; Kashaninia 2008) were of the same study, so that only one was included and it counted as one of the 19 unique studies.

 

Included studies

The 19 included studies reported on a total of 1594 infants. Among the included studies, four were with full term neonates (Gray 2000; Sajedi 2007; Chermont 2009; Saeidi 2011) and the remaining 15 were with preterm neonates (Johnston 2003; Ludington-Hoe 2005; Castral 2008; Freire 2008; Johnston 2008; Kostandy 2008; Akcan 2009; Cong 2009; Johnston 2009; Okan 2010; Cong 2011; Johnston 2011; Cong 2012; Johnston 2012; Nimbalkar 2013). Details of each study are outlined in the tables under Characteristics of included studies.

Most (15) of the included studies examined responses to the painful procedure of heel lance (Gray 2000; Johnston 2003; Ludington-Hoe 2005; Freire 2008; Castral 2008; Johnston 2008; Kostandy 2008; Cong 2009; Johnston 2009; Okan 2010; Cong 2011; Johnston 2011; Cong 2012; Johnston 2012; Nimbalkar 2013) and are shown in  Table 1. Three studies (Sajedi 2007; Chermont 2009; Saeidi 2011) examined the response to intramuscular injection ( Table 2) and one study (Akcan 2009) included both venipuncture and heel lance ( Table 3).

Outcome measures were varied among studies, with many including more than one. Physiological measures included heart rate during the painful procedure (Gray 2000; Johnston 2003; Ludington-Hoe 2005; Sajedi 2007; Castral 2008; Johnston 2008; Freire 2008; Cong 2009; Okan 2010; Cong 2012; Nimbalkar 2013) and after the painful procedure (Gray 2000; Ludington-Hoe 2005; Sajedi 2007; Castral 2008; Johnston 2008; Cong 2009; Cong 2012); heart rate recovery (time to return to baseline levels post-procedure (Johnston 2008; Johnston 2009; Johnston 2011; Johnston 2012)); spectral analysis of electrocardiogram (ECG) signals of low frequency spectrum, high frequency spectrum, and low-to-high frequency ratio (Cong 2009; Cong 2012); transcutaneous oxygen saturation levels (Johnston 2003; Ludington-Hoe 2005; Sajedi 2007; Johnston 2008; Okan 2010; Saeidi 2011); respiratory rate (Ludington-Hoe 2005); and salivary cortisol levels (Cong 2011). Behavioural state was used in two studies (Ludington-Hoe 2005; Cong 2009). Cry duration was an outcome for five studies (Gray 2000; Ludington-Hoe 2005; Kostandy 2008; Okan 2010; Saeidi 2011). Facial grimacing, not according to a validated measure, was used in two studies (Gray 2000; Okan 2010), while in three others the validated Neonatal Facial Coding Scale (NFCS) was used (Castral 2008; Chermont 2009; Okan 2010). Validated composite pain measures that included both physiological and behavioural indicators were used in 13 studies. The Premature Infant Pain Profile (PIPP) was used in 10 studies (Johnston 2003; Freire 2008; Johnston 2008; Akcan 2009; Johnston 2009; Chermont 2009; Cong 2011; Johnston 2011; Johnston 2012; Nimbalkar 2013), and the Neonatal Infant Pain Scale (NIPS) was used in three studies (Sajedi 2007; Chermont 2009; Saeidi 2011).

 

Excluded studies

Of the 19 studies that were excluded, two focused on breastfeeding (Uga 2008; Abdel-Razek 2009), four did not have SSC as defined in this review (Bellieni 2002; Arditi 2006; Bellieni 2007; Vivancos 2010), and three did not have ventral skin contact as a part of their SSC intervention (Reis 2003; Axelin 2009; Campbell-Yeo 2012). Maternal interview was the focus of one study (Silva 2004). One study used maternal voice without actual contact (Johnston 2007b) while another used neurobehavioural scores (NIDCAP) associated with pain, which are not validated as a pain measure (Ferber 2008). One study, Kashaninia 2008, was a duplicate of another (Sajedi 2007). Finally, seven studies reported on SSC alone without implementation of a painful procedure (Mooncey 1997; Gazzolo 2000; Morelius 2005; Miles 2006; Erlandsson 2007; Gabriel 2010; Schlez 2011).

 

Risk of bias in included studies

The risk of bias for each study may be seen under Characteristics of included studies and as percentages across all included studies in Figure 1.

 FigureFigure 1. Risk of bias graph: review authors' judgements about each risk of bias item presented as percentages across all included studies.

 

Allocation

Random sequence generation, a procedure to avoid selection bias, was adequate in 11 studies. Allocation concealment, another source of selection bias, was deemed adequate for eight studies.

 

Blinding

Blinding to avoid performance or detection bias was adequate in only five of the studies. Although 13 of the remaining trials did institute measures to overcome detection bias, the outcomes were assessed either by monitoring equipment or by persons naive to the intervention, so some uncertainty remained especially when video observations were made. Only two studies specifically mentioned how they dealt with blinding the observers.

 

Incomplete outcome data

Incomplete outcome data were rated above low risk in only four studies.

 

Selective reporting

Reporting was adequate in all but three studies. Two were unclear and one study's parameters as reported in the trial registry were not included in the report.

 

Other potential sources of bias

There were three individual cases of other bias: there was a combination of two data sets, different times for the painful procedure by group were not included in the regression analysis, and consent was obtained after randomisation. Four other studies had unclear potential bias. In one, there was some potential for inconsistency among sites regarding sucrose use in the usual care group. A power calculation was not reported in one study, and the washout period was not described in the two others.

 
Heterogeneity results

There were many outcomes for which heterogeneity could not be measured via the I2 statistic, that is, where only one study reported an outcome such as change in heart rate or change in oxygen saturation. When the I2 statistic could be calculated the results showed a wide range, with the physiological outcomes having I2 values of 0% and some composite measures having values over 50%, for example, PIPP at 30 seconds following heel lance versus control, I2 = 79%.

 

Effects of interventions

Inconsistencies in the outcomes prevented all studies from being included in meta-analyses. Each study is thus reported separately and appears in  Table 1 and  Table 2 below, grouped according to the painful intervention.

 
1. Effectiveness of skin-to-skin care (SSC) compared to incubator control (Comparison 1)

 
1.1 Heart rate response

Eleven studies examined heart rate during the heel lance procedure (Gray 2000; Johnston 2003; Ludington-Hoe 2005; Sajedi 2007; Castral 2008; Freire 2008; Johnston 2008; Cong 2009; Okan 2010; Cong 2012; Nimbalkar 2013). Johnston 2008 reported the average heart rate to be significantly lower at 30 (P < 0.01), 60 (P < 0.01), and 90 (P < 0.05) seconds post-heel lance. Only four studies could be combined in an analysis (Castral 2008; Cong 2009; Ludington-Hoe 2005; Cong 2012) since results of the first condition only were not reported in cross-over designs, and not all authors responded to requests for the data for the first condition separately. As well, the duration of time for which the heart rate was collected either varied between studies or was not reported. Finally, when authors did respond, the calculations were conducted differently (that is, maximum, not mean heart rate was acquired). Cong 2012 reported two studies in the same manuscript, one of SSC for 30 minutes and one of SSC for 15 minutes. One other study, Sajedi 2007, examined heart rate during intramuscular injection and reported lower scores, that is, in favour of SSC. Johnston 2003 reported no overall differences, Johnston 2008 provided unpublished data for the first condition on maximum heart rate with significant differences in favour of SSC. Okan 2010 reported the median heart rate for SSC plus breast feeding, SSC alone, and control, and found significantly higher heart rate in the control but similar levels in the two intervention groups. Nimbalkar 2013 reported change in pulse, which significantly favoured SSC, but this was for the total sample and was not for the first condition separately in the cross-over design.

The meta-analysis showed differences between the experimental and control groups ranging from 0.57 to 2.3 beats per minute with a non-significant MD of 0.35 (95% CI -6.01 to 6.71) beats per minute ( Analysis 1.1).

 
1.2 Heart rate recovery

Heart rate following the painful procedure was reported in five studies, but only four could be entered into the analysis (Ludington-Hoe 2005; Castral 2008; Cong 2009; Cong 2012, note the latter report contains two studies). The MD was non-significant at -3.73 (95% CI -8.86 to 1.39) ( Analysis 1.2). The remaining studies (Gray 2000; Cong 2009) favoured SSC. Johnston 2008 reported that the time to return to baseline heart rate following the application of the adhesive bandage (signifying the end of blood sampling) was significantly faster at 123 seconds (95% CI 103 to 142) for the KC condition and 193 seconds for the incubator condition (95% CI 158 to 227; F (61, 1) = 13.6, P < 0.0000).

 
1.3 Heart rate variability

Two studies reported heart rate variability as an outcome (Cong 2009; Cong 2012). Both studies had a cross-over design and the first condition was separated out for this review. In Cong 2009, the low frequency/high frequency (LF/HF) ratio was lower at heel stick than with SSC, although it was lower in SSC during other phases of the procedure, particularly recovery. Both HF and LF were higher in the SSC condition so that across most phases of the procedure SSC was favoured. In Cong 2012, infants were randomly ordered into 15 minutes of SSC, 30 minutes of SSC, and incubator control. The heart rate variability results were non-significantly different among the conditions.

 
1.4 Oxygen saturation during painful procedure

Three studies used oxygen saturation as an outcome (Ludington-Hoe 2005; Sajedi 2007; Johnston 2008), however they could not be combined for analysis. Although Ludington-Hoe 2005 and Johnston 2008 examined preterm neonates undergoing heel lance, one reported values averaged over the duration of the procedure while the other reported values averaged over 30 second epochs post-lance for the duration of the procedure. The other study, Sajedi 2007, examined full term neonates receiving intramuscular injection. Ludington-Hoe 2005 did not find significant differences between SSC and incubator care. Johnston 2008 found that the average oxygen saturation levels were significantly higher at 60 (P < 0.01) and 90 (P < 0.05) seconds post-heel lance compared to incubator controls. Sajedi 2007 reported an almost 4% lower oxygen saturation (P < 0.001) in the control group, favouring SSC.

 
1.5 Oxygen saturation after painful procedure

The same studies as above (Ludington-Hoe 2005; Sajedi 2007) as well as Saeidi 2011 also reported oxygen saturation at the end of the painful procedure. Sajedi 2007 reported a significant 2.8% higher oxygen saturation in the SSC group, but the Ludington-Hoe 2005 study showed wide variance with a similar magnitude of difference which was not significant. Saeidi 2011 reported non-significant differences in oxygen saturation.

 
1.6 Change in oxygen saturation

Only one study examined change in oxygen saturation (Freire 2008), in which the difference was not significant between SSC and standard care control ( Table 1). Nimbalkar 2013's raw data showed a difference in oxygen saturation but following the Bonferroni correction this was not significant.

 
1.7 Serum cortisol

Only one study (Cong 2011) examined serum cortisol level, comparing 80 minutes and 30 minutes of SSC with a standard care control. The study showed significantly higher serum cortisol levels in the 80 minute SSC group (mean ± SD: 5.73 ± 1.97) than the standard care control group (mean ± SD: 5.32 ± 1.72), P > 0.05. Conversely, serum cortisol levels were lower in the 30 minute SSC group (mean ± SD: 5.63 ± 2.30) than the standard care control group (mean ± SD: 9.15 ± 6.59), P < 0.05 ( Table 1).

 
1.8 Salivary cortisol

Only one study used salivary cortisol levels as an outcome (Cong 2011 (Study 1 and 2)). There were two subsamples in that study, one receiving SSC for 80 minutes and the other for 30 minutes. There were significantly higher salivary cortisol levels in the 80 minute SSC group (mean ± SD: 0.19 ± 0.10) than the standard care control group (mean ± SD: 0.15 ± 0.06), P > 0.05. Conversely, salivary cortisol levels were lower in the 30 minute SSC group (mean ± SD: 0.21 ± 0.12) than the standard care control group (mean ± SD: 0.57 ± 0.61), P < 0.05 ( Table 1).

 
1.9 Premature Infant Pain Profile (PIPP) at 30 seconds

Five studies used the PIPP as the outcome for heel lance (Johnston 2003; Freire 2008; Johnston 2008; Akcan 2009; Cong 2011 (Study 1 and 2)). Cong 2011 was analysed for the two amounts of time of SSC so that the first study of 80 minutes SSC was entered first and the second study of SSC for 30 minutes was entered second, although both are listed as Cong 2011. The PIPP was reported in 30 second blocks from the time of the heel lance. At 30 seconds, based on analyses of four of the studies (Johnston 2003; Freire 2008; Johnston 2008; Cong 2011), there was a significant effect in favour of SSC (MD -3.21, 95% CI -3.94 to -2.48), although Cong 2011 (study 1) and Johnston 2008 did not find a significant difference ( Analysis 1.9).

 
1.10 PIPP scores at 60 seconds

Three studies used the PIPP as an outcome for heel lance (Johnston 2003; Johnston 2008; Cong 2011 (Study 1 and 2)) and one used it as an outcome for heel lance or venipuncture (Akcan 2009). There was a significant difference in favour of SSC in the analysis of heel lance (MD -1.85, 95% CI -3.03 to -0.68), and again Johnston 2008 and Cong 2011 (Study 1) did not find a significant difference ( Analysis 1.10).

 
1.11 PIPP at 90 seconds

There was a significant difference in favour of SSC with three studies (Johnston 2003; Johnston 2008; Cong 2011 (Study 2)) for the PIPP score at 90 seconds (MD -1.34, 95% CI -2.56 to -0.13) ( Analysis 1.11).

 
1.12 PIPP at 120 seconds

Three studies used the PIPP at 120 seconds as an outcome for heel lance (Johnston 2003; Johnston 2008; Cong 2011) and one used it as an outcome for heel lance or venipuncture (Akcan 2009). There was an MD of 0.04 (95% CI -1.14 to 1.23), reflecting no significant difference ( Analysis 1.12).

 
1.13 PIPP following end of procedure

One report, Cong 2011 (two studies of 80 and 30 minutes SSC), followed PIPP scores beyond the time of the procedure. In both studies the PIPP scores favoured SSC, measured in 30 second blocks for two minutes following the procedure, by between 8.12 and 0.4 points on the PIPP. The closer to the end of the procedure the greater the difference was in scores.

 
1.14 Neonatal Facial Coding System (NFCS) during painful procedure

One study used the NFCS as an outcome for heel lance on preterm neonates (Castral 2008), and another used it as an outcome in full term neonates for intramuscular injection (Chermont 2009). In Castral 2008 there was a mean difference of 1.872 in favour of SSC (P < 0.001). There was no difference between skin-to-skin alone and the standard care control in Chermont 2009.

 
1.15 NFCS at recovery

Similarly, at recovery one study used the NFCS as an outcome for heel lance in preterm neonates (Castral 2008) and another for intramuscular injection in full term neonates (Chermont 2009). Both studies favoured SSC.

 
1.16 Duration of crying after painful procedure

Four studies included cry duration as an outcome, which ranged from 19 seconds to 0.73 seconds but was not significantly different between the experimental and control groups (MD -0.93, 95% CI -2.28 to 0.42). This analysis was based on only two studies (Ludington-Hoe 2005; Kostandy 2008) since the other two studies did not provide enough information to include their results in the analysis (Gray 2000; Okan 2010).

 
1.17 Neonatal Infant Pain Scale (NIPS)

Chermont 2009, Saeidi 2011, Sajedi 2007 (as reported in the same study by Kashaninia 2008) used the NIPS as an outcome. In Chermont 2009, at the time of the actual intramuscular injection SSC alone was no better than control, but it was better at recovery. In Kashaninia 2008, the NIPS, a scale used to generate interval data, was reported as ordinal data and more infants in the SSC group were in the 'no pain to mild' category. Similarly, Saeidi 2011 reported results as the percentage of participants in each group having NIPS scores of 6 or 7 during the vaccination, which significantly favoured SSC with 96% of controls with a score of 7 versus only 70% in the SSC group.

 
1.18 Sleep and wake state

Four studies reported on sleep and wake state (Ludington-Hoe 2005; Sajedi 2007; Cong 2009; Cong 2012). Since this is a categorical or ordinal outcome, no analysis was performed. One study, Sajedi 2007, was conducted with full term neonates while the others were with preterm neonates. There were no differences in sleep and wake state at the time of the invasive procedure, although Cong 2012 reported more infants in the SSC group in quiet sleep during recovery following the procedure, as did Ludington-Hoe 2005 who reported that infants in SSC were more likely to be in deep sleep during baseline and heel warming. Kashaninia 2008 reported state as a dichotomous outcome, fussy or any other state, and reported a higher proportion of infants to be in a 'fussy' state in the control condition.

 
2. Effectiveness of skin-to-skin care (SSC) with different providers (Comparison 2)

Two studies compared different providers of SSC (Johnston 2011; Johnston 2012), although Johnston 2012 was reported only as a pilot study aimed at examining feasibility and effect size ( Table 4). Since both studies examined preterm neonates undergoing heel lance and used PIPP scores at 30 second intervals over two minutes following the heel lance as well as heart rate recovery (defined as time for the heart rate to return to baseline levels) they were entered into a comparison. Differences in heart rate recovery were not significant (MD -32.58, 95% CI -92.43 to 27.26) in spite of the large mean difference in favour of the mother, due mostly to high variation. PIPP scores similarly had large mean differences favouring the mother but the variance was also large so that any difference was non-significant.

 
3. Effectiveness of skin-to-skin care (SSC): analysis by duration of SSC

Cong 2009 and Cong 2012 reported results from different durations of SSC, the first comparing 80 to 30 minutes SSC and the second comparing 30 to 15 minutes. Both studies examined preterm neonates undergoing heel lance and some physiological outcomes were the same so that an analysis was able to be performed.

 
4. Effectiveness of skin-to-skin care (SSC) compared to alternative treatments

There were no studies that could be combined for analysis. There were some interesting comparisons that are described below.

 
SSC versus sweet taste

The study by Chermont 2009 on full term newborns receiving an intramuscular injection compared SSC alone or in combination with dextrose to incubator controls. On the PIPP outcome, SSC was most effective with or without the addition of dextrose. On the NFCS and NIPS, SSC was favoured over dextrose or control, although the combination was most effective. Freire 2008 also compared SSC with sweet taste (glucose) to control in preterm neonates undergoing heel lance, with the PIPP score. Heart rate and oxygen saturation variability (not defined) were reported to significantly favour SSC over both control and glucose. This was also reported for the composite measure of these variables, the PIPP. All outcomes favoured SSC.

 
SSC versus breastfeeding

Okan 2010 compared SSC to breastfeeding or swaddled control in full term neonates undergoing heel lance. In all outcomes (heart rate, oxygen saturation, NFCS, and duration of crying) there were no differences between SSC or breastfeeding, but both were better than the swaddled control group.

 
SSC versus enhanced SSC

One study, Johnston 2009, examined PIPP scores in preterm neonates undergoing heel lance for differences between SSC and SSC enhanced by the mother rocking, singing and offering the infant a finger or pacifier for sucking. There were no differences between the conditions.

 
5. Effectiveness of skin-to-skin care (SSC): analysis by dose or duration of SSC

The range of time for SSC prior to the intervention was two minutes (Saeidi 2011) to three hours (Ludington-Hoe 2005). The only studies that compared times were Cong 2009 and Cong 2011. However, these studies used different outcomes and thus no analyses could be conducted. In Cong 2009, 80 minute SSC and 30 minute SSC were independently compared to control for the physiological variables of heart rate and heart rate variability. SSC was favoured only in the 30 minute condition. In Cong 2011, the PIPP was used as an outcome for SSC for 15 minutes, SSC for 30 minutes, or control. The 30 minute SSC was favoured over control and 15 minute SSC. Although these two studies, not directly compared, seemed to favour 30 minutes to either longer or shorter doses, other studies using different outcomes favoured (or did not favour) SSC for times longer and shorter than 30 minutes so no conclusion could be made.

 
6. Effectiveness of skin-to-skin care (SSC): analysis by postmenstrual age (PMA)

Outcomes of studies reporting different PMAs were different so that comparisons could not be made. Studies examined different times and some used the same outcomes (for example, PIPP) but the comparisons and painful procedures were different so that an effect size could not be estimated.

 

Discussion

  1. Top of page
  2. Background
  3. Objectives
  4. Methods
  5. Results
  6. Discussion
  7. Authors' conclusions
  8. Acknowledgements
  9. Data and analyses
  10. Contributions of authors
  11. Declarations of interest
  12. Sources of support
  13. Index terms
 

Summary of main results

In this first review of skin-to-skin care (SSC) for procedural pain in neonates, 19 studies were found that met the selection criteria of using SSC as an intervention to reduce pain. Most of the studies used the most common painful event of heel lance as the painful procedure, although venipuncture and intramuscular injections were also among the painful procedures. Very few studies could be compared due to variations in painful procedure, design, outcomes, or participants.

The most detailed information was found in studies with preterm neonates undergoing heel lance for SSC versus control with either heart rate, heart rate variability, or the composite measure PIPP as outcomes. The physiological outcomes of heart rate during or after the procedure or heart rate variability, low frequency, high frequency, or low/high frequency ratio spectra, were not significant for either SSC or control. The heterogeneity was small in these studies. The PIPP in the first 90 seconds favoured SSC but the heterogeneity was high.

Two studies examined different providers of SSC and were able to be entered into an analysis for the PIPP and heart rate recovery. The differences between mother provider and other provider were not significant.

No analyses could be conducted on the effect on outcomes of duration of SSC or different age groups of infants.

 

Overall completeness and applicability of evidence

These results were based on a small number of studies as there was wide variability in outcomes reported. Some outcomes could not be analysed. For example, Castral 2008 reported a significant difference in facial actions favouring SSC for heel lance, but there was not enough information to include it in an analysis. Although Chermont 2009 also used facial actions as an outcome, the painful procedure of that study was intramuscular injection. Both studies reported results favouring SSC but they could not be analysed together. 

Although it would be of interest to know if there was a dose-response relationship, that is, did the number of minutes in SSC increase the effectiveness, we were not able to conduct that analysis. We were not even able to make a direct comparison of differences with 30 minutes as a cut-off point. Ludington-Hoe 2005 reported the longest duration of SSC prior to the painful event of three hours, and Saeidi 2011 reported the shortest duration of two minutes. Both of these studies reported results favouring SSC but no comparisons could be made. One study, Cong 2011, reported on two samples, one receiving 60 minutes of SSC and the other only 10 minutes, and both were compared to standard care. There were positive results only for the group receiving 10 minutes of SSC, reported as lower PIPP scores as well as lower serum and salivary cortisol levels.

The providers of SSC were compared in two studies, which showed mean differences in favour of the mother, but the variance was very large so there were no significant differences. Only three studies included full term neonates and one was for heel lance, for which standard deviations were not available (Gray 2000). The other two studies (Sajedi 2007; Chermont 2009) used intramuscular injection rather than heel lance so that a comparison between full term neonates and preterm neonates was not possible. 

No studies reported any adverse events.

 

Quality of the evidence

The studies that were included were generally strong and free from bias. More than half (11/19) of the studies reported using adequate random allocation, and most reported low risk of bias related to incomplete data (15/19), selective reporting (16/19), and other forms of possible bias (12/19). Just under half of the studies (8/19) reported adequate allocation concealment and blinding (5/19). Thirteen of the studies did report measures such as blinded assessors using objective outcome measures and 'close up video recording of infant faces', but few addressed the issue of whether the presence of the mother may have been detectable to the assessor. Little information was provided regarding the 'usual care' control, so in the first comparison of SSC versus no-treatment control we were uncertain precisely what the control condition was.

The degree of heterogeneity of the studies varied a great deal, but interestingly the more heterogeneous outcomes were physiological. There is a greater potential for bias in behavioural outcomes that require human judgement. Only a few studies reported how video recordings avoided identification of the condition. The conflicting results between physiological outcomes, mostly showing no differences, and composite or behavioural outcomes generally favouring SSC would suggest caution in interpretation. Further research is needed in order to solve the long standing confusion and controversy about which indicators are most appropriate.

 

Potential biases in the review process

Two of the authors of this review (CJ, MCY) authored studies that were reviewed (Johnston 2003; Johnston 2008; Johnston 2009; Johnston 2011; Johnston 2012). Another author (AF) studied SSC for her doctoral dissertation and a manuscript is under review. Inglis is a nurse manager who champions SSC in the nurseries at the IWK Health Centre.

 

Agreements and disagreements with other studies or reviews

There have been a few reviews of non-pharmacological interventions for procedural pain relief in neonates (Cignacco 2007; Yamanda 2008; Warnock 2010; Pillai Riddell 2011) and all support the practice of SSC (also known as Kangaroo Care (KC)). No studies or reviews were found that disagreed.

 

Authors' conclusions

  1. Top of page
  2. Background
  3. Objectives
  4. Methods
  5. Results
  6. Discussion
  7. Authors' conclusions
  8. Acknowledgements
  9. Data and analyses
  10. Contributions of authors
  11. Declarations of interest
  12. Sources of support
  13. Index terms

 

Implications for practice

Only a few data sets could be pooled, thus not enabling an effect size to be determined on all but a few outcomes. Nevertheless studies comparing skin-to-skin care to standard care, which was rarely defined, favoured skin-to-skin care or were non-significant. No studies favoured standard care. In the two studies comparing skin-to-skin care to glucose, skin-to-skin care was more effective in one study and a possible synergistic effect was reported in the other. The addition of breastfeeding did not appear to increase the effectiveness of SSC. When skin-to-skin care was enhanced by the addition of the mother's voice or rocking, it had no additional benefit. There were no adverse events reported in any of the studies. Therefore, it would seem that for neonates who are able to be held in the skin-to-skin care paradigm, using it for the painful procedures of heel lance, venipuncture, and intramuscular injection is potentially beneficial and not harmful. However, the degree of benefit, although not estimable, may not be large.

 
Implications for research

There are numerous areas in this topic that require further research before definitive statements can be made. First of all, more studies are needed that use outcomes that are the same as the ones in this review so that an effect size can be estimated. Secondly, studies need to be more rigorous about randomisation, allocation concealment, and blinding. Thirdly, when wide age ranges are used, particularly when full term and preterm neonates are in the same study, results for each group should be reported separately. Although it seems as though a 'dose' as low as 10 minutes was effective, more studies testing different durations of the provision of skin-to-skin care might allow for a dose response analysis to be conducted. All the studies were conducted using skin-to-skin care for a single procedure. It would be interesting to determine if the effect changed with repeated use. Once more studies meet these criteria, studies on dose, that is, duration of skin-to-skin care, and other providers would be of interest. More fundamentally, it would be of interest to explore the underlying mechanism of the comforting effect of skin-to-skin care and its long-term impact.

 

Acknowledgements

  1. Top of page
  2. Background
  3. Objectives
  4. Methods
  5. Results
  6. Discussion
  7. Authors' conclusions
  8. Acknowledgements
  9. Data and analyses
  10. Contributions of authors
  11. Declarations of interest
  12. Sources of support
  13. Index terms

The Quebec Interuniversity Nursing Intervention Research Group (GRISIIQ) provided direct funding for this review. Indirect funding was from Fonds de la recherche en santé du Quebéc (FRSQ), Canadian Institutes of Health Research (CIHR), Nova Scotia Health Research Foundation (NSHRF).

 

Data and analyses

  1. Top of page
  2. Background
  3. Objectives
  4. Methods
  5. Results
  6. Discussion
  7. Authors' conclusions
  8. Acknowledgements
  9. Data and analyses
  10. Contributions of authors
  11. Declarations of interest
  12. Sources of support
  13. Index terms
Download statistical data

 
Comparison 1. Skin-to-skin care versus control

Outcome or subgroup titleNo. of studiesNo. of participantsStatistical methodEffect size

 1 Heart Rate during painful procedure4121Mean Difference (IV, Fixed, 95% CI)0.35 [-6.01, 6.71]

    1.1 Heel lance
4121Mean Difference (IV, Fixed, 95% CI)0.35 [-6.01, 6.71]

 2 Heart rate following painful procedure4121Mean Difference (IV, Fixed, 95% CI)-3.73 [-8.86, 1.39]

    2.1 Heel lance
4121Mean Difference (IV, Fixed, 95% CI)-3.73 [-8.86, 1.39]

 3 HRV during painful procedure - Low frequency power238Mean Difference (IV, Fixed, 95% CI)-2.11 [-17.69, 13.47]

    3.1 Heel lance
238Mean Difference (IV, Fixed, 95% CI)-2.11 [-17.69, 13.47]

 4 HRV during painful procedure - High frequency power238Mean Difference (IV, Fixed, 95% CI)-5.11 [-23.36, 13.14]

    4.1 Heel lance
238Mean Difference (IV, Fixed, 95% CI)-5.11 [-23.36, 13.14]

 5 HRV during painful procedure - Low frequency to high frequency ratio238Mean Difference (IV, Fixed, 95% CI)2.33 [-2.94, 7.59]

    5.1 Heel lance
238Mean Difference (IV, Fixed, 95% CI)2.33 [-2.94, 7.59]

 6 HRV after painful procedure - Low frequency power238Mean Difference (IV, Fixed, 95% CI)0.58 [-0.92, 2.07]

    6.1 Heel lance
238Mean Difference (IV, Fixed, 95% CI)0.58 [-0.92, 2.07]

 7 HRV after painful procedure - High frequency power238Mean Difference (IV, Fixed, 95% CI)0.05 [-0.18, 0.29]

    7.1 Heel lance
238Mean Difference (IV, Fixed, 95% CI)0.05 [-0.18, 0.29]

 8 HRV during painful procedure - Low frequency to high frequency ratio238Mean Difference (IV, Fixed, 95% CI)-3.77 [-13.69, 6.14]

    8.1 Heel lance
238Mean Difference (IV, Fixed, 95% CI)-3.77 [-13.69, 6.14]

 9 PIPP Score 30 seconds after painful procedure5268Mean Difference (IV, Fixed, 95% CI)-3.21 [-3.94, -2.48]

    9.1 Heel lance
5268Mean Difference (IV, Fixed, 95% CI)-3.21 [-3.94, -2.48]

 10 PIPP Score 60 seconds after painful procedure3164Mean Difference (IV, Fixed, 95% CI)-1.85 [-3.03, -0.68]

    10.1 Heel lance
3164Mean Difference (IV, Fixed, 95% CI)-1.85 [-3.03, -0.68]

 11 PIPP Score 90 seconds after painful procedure3163Mean Difference (IV, Fixed, 95% CI)-1.34 [-2.56, -0.13]

    11.1 Heel lance
3163Mean Difference (IV, Fixed, 95% CI)-1.34 [-2.56, -0.13]

 12 PIPP Score 120 seconds after painful procedure3157Mean Difference (IV, Fixed, 95% CI)0.04 [-1.14, 1.23]

    12.1 Heel lance
3157Mean Difference (IV, Fixed, 95% CI)0.04 [-1.14, 1.23]

 
Comparison 2. Skin-to-skin care with different providers

Outcome or subgroup titleNo. of studiesNo. of participantsStatistical methodEffect size

 1 Heart rate recovery278Mean Difference (IV, Fixed, 95% CI)-32.97 [-94.52, 28.59]

    1.1 Father
162Mean Difference (IV, Fixed, 95% CI)-26.0 [-91.34, 39.34]

    1.2 Alternate Female
116Mean Difference (IV, Fixed, 95% CI)-88.0 [-271.66, 95.66]

 2 PIPP Score 30 seconds280Mean Difference (IV, Fixed, 95% CI)-1.29 [-2.73, 0.16]

    2.1 Father
162Mean Difference (IV, Fixed, 95% CI)-0.94 [-2.56, 0.68]

    2.2 Alternate Female
118Mean Difference (IV, Fixed, 95% CI)-2.63 [-5.82, 0.56]

 3 PIPP Score 60 seconds280Mean Difference (IV, Fixed, 95% CI)0.79 [-0.75, 2.34]

    3.1 Father
162Mean Difference (IV, Fixed, 95% CI)1.30 [-0.37, 2.97]

    3.2 Alternate Female
118Mean Difference (IV, Fixed, 95% CI)-2.13 [-6.15, 1.89]

 4 PIPP Score 90 seconds280Mean Difference (IV, Fixed, 95% CI)-0.48 [-2.05, 1.09]

    4.1 Father
162Mean Difference (IV, Fixed, 95% CI)0.0 [-1.73, 1.73]

    4.2 Alternate Female
118Mean Difference (IV, Fixed, 95% CI)-2.62 [-6.27, 1.03]

 5 Pipp Score 120 Seconds280Mean Difference (IV, Fixed, 95% CI)0.12 [-1.31, 1.55]

    5.1 Father
162Mean Difference (IV, Fixed, 95% CI)0.61 [-0.93, 2.15]

    5.2 Alternate Female
118Mean Difference (IV, Fixed, 95% CI)-2.88 [-6.70, 0.94]

 

Contributions of authors

  1. Top of page
  2. Background
  3. Objectives
  4. Methods
  5. Results
  6. Discussion
  7. Authors' conclusions
  8. Acknowledgements
  9. Data and analyses
  10. Contributions of authors
  11. Declarations of interest
  12. Sources of support
  13. Index terms

CJ oversaw the process and arbitrated disputes between other reviewers, and wrote narrative. MCY and RZ contributed to content and editing of narrative.
MCY, AF, DI, RZ reviewed articles and rated them according to criteria.
DS served as methodological expert and advised about statistics.

 

Declarations of interest

  1. Top of page
  2. Background
  3. Objectives
  4. Methods
  5. Results
  6. Discussion
  7. Authors' conclusions
  8. Acknowledgements
  9. Data and analyses
  10. Contributions of authors
  11. Declarations of interest
  12. Sources of support
  13. Index terms

The authors have nothing to declare.

 

Sources of support

  1. Top of page
  2. Background
  3. Objectives
  4. Methods
  5. Results
  6. Discussion
  7. Authors' conclusions
  8. Acknowledgements
  9. Data and analyses
  10. Contributions of authors
  11. Declarations of interest
  12. Sources of support
  13. Index terms
 

Internal sources

  • GRISIIQ, Canada.

 

External sources

  • Eunice Kennedy Shriver National Institute of Child Health and Human Development National Institutes of Health, Department of Health and Human Services, USA.
    Editorial support of the Cochrane Neonatal Review Group has been funded with Federal funds from the Eunice Kennedy Shriver National Institute of Child Health and Human Development National Institutes of Health, Department of Health and Human Services, USA, under Contract No. HHSN275201100016C.

References

References to studies included in this review

  1. Top of page
  2. AbstractRésumé
  3. Background
  4. Objectives
  5. Methods
  6. Results
  7. Discussion
  8. Authors' conclusions
  9. Acknowledgements
  10. Data and analyses
  11. Contributions of authors
  12. Declarations of interest
  13. Sources of support
  14. Characteristics of studies
  15. References to studies included in this review
  16. References to studies excluded from this review
  17. References to studies awaiting assessment
  18. Additional references
Akcan 2009 {published data only}
  • Akcan E, Yiğit R, Atici A. The effect of kangaroo care on pain in premature infants during invasive procedures. Turkish Journal of Pediatrics 2009;51(1):14-8.
Castral 2008 {published and unpublished data}
Chermont 2009 {published and unpublished data}
  • Chermont AG, Falcão LF, de Souza Silva EH, de Cássia Xavier Balda R, Guinsburg R. Skin-to-skin contact and/or oral 25% dextrose for procedural pain relief for term newborn infants. Pediatrics 2009;124(6):e1101-7.
Cong 2009 {published and unpublished data}
  • Cong X, Ludington-Hoe SM, McCain G, Fu P. Kangaroo care modifies preterm infant heart rate variability in response to heel stick pain: Pilot study. Early Human Development 2009;85(9):561-7.
Cong 2011 {published and unpublished data}
  • Cong X, Ludington-Hoe SM, Walsh S. Randomized crossover trial of kangaroo care to reduce biobehavioural pain responses in preterm infants: a pilot study. Biological Research for Nursing 2011;13(2):204-16.
Cong 2012 {published data only}
  • Cong X, Cusson RM, Walsh S, Hussain N, Ludington-Hoe SM, Zhang D. Effects of skin-to-skin contact on autonomic pain responses in preterm infants. The Journal of Pain 2012;13(7):636-45.
Freire 2008 {published and unpublished data}
Gray 2000 {published data only}
Johnston 2003 {published and unpublished data}
  • Johnston CC, Stevens B, Pinelli J, Gibbins S, Filion F, Jack A, et al. Kangaroo care is effective in diminishing pain response in preterm neonates. Archives of Pediatrics & Adolescent Medicine 2003;157(11):1084-8.
Johnston 2008 {published and unpublished data}
  • Johnston CC, Filion F, Campbell-Yeo M, Goulet C, Bell L, McNaughton K, et al. Kangaroo mother care diminishes pain from heel lance in very preterm neonates: a crossover trial. BMC Pediatrics 2008;8:13.
Johnston 2009 {published and unpublished data}
  • Johnston CC, Filion F, Campbell-Yeo M, Goulet C, Bell L, McNaughton K, et al. Enhanced kangaroo mother care for heel lance in preterm neonates: a crossover trial. Journal of Perinatology 2009;29(1):51-6.
Johnston 2011 {published and unpublished data}
  • Johnston CC, Campbell-Yeo M, Filion F. Paternal vs maternal kangaroo care for procedural pain in preterm neonates: A randomized crossover trial. Archives of Pediatrics & Adolescent Medicine 2011;165(9):792-6.
Johnston 2012 {published and unpublished data}
Kostandy 2008 {published data only}
  • Kostandy RR, Ludington-Hoe SM, Cong X, Abouelfettoh A, Bronson C, Stankus A, et al. Kangaroo Care (skin contact) reduces crying response to pain in preterm neonates: pilot results. Pain Management Nursing 2008;9(2):55-65.
Ludington-Hoe 2005 {published data only}
  • Ludington-Hoe SM, Hosseini R, Torowicz DL. Skin-to-skin contact (kangaroo care) analgesia for preterm infant heel stick. AACN Clinical Issues: Advanced Practice in Acute and Critical Care 2005;16(3):373-87.
Nimbalkar 2013 {published and unpublished data}
  • Nimbalkar SM, Chaudhary NS, Gadhavi KV, Phatak A. Kangaroo mother care in reducing pain in preterm neonates on heel prick. Indian Journal of Pediatrics 2013;80(1):6-10.
Okan 2010 {published data only (unpublished sought but not used)}
  • Okan F, Ozdil A, Bulbul A, Yapici Z, Nuhoglu A. Analgesic effects of skin-to-skin contact and breastfeeding in procedural pain in healthy term neonates. Annals of Tropical Paediatrics 2010;30(2):119-28.
Saeidi 2011 {published data only}
  • Saeidi R, Asnaashari Z, Amirnejad M, Esmaeili H, Robatsangi MG. Use of "Kangaroo Care" to alleviate the intensity of vaccination pain in newborns. Iranian Journal of Pediatrics March 2011;21(1):99-102.
Sajedi 2007 {published data only}
  • Sajedi F, Kashaninia Z, Rahgozar M, Noghabi FA. The effect of Kangaroo Care on physiologic responses to pain of an intramuscular injection in neonates. Iranian Journal of Pediatrics 2007;17(4):339-44.

References to studies excluded from this review

  1. Top of page
  2. AbstractRésumé
  3. Background
  4. Objectives
  5. Methods
  6. Results
  7. Discussion
  8. Authors' conclusions
  9. Acknowledgements
  10. Data and analyses
  11. Contributions of authors
  12. Declarations of interest
  13. Sources of support
  14. Characteristics of studies
  15. References to studies included in this review
  16. References to studies excluded from this review
  17. References to studies awaiting assessment
  18. Additional references
Abdel-Razek 2009 {published data only}
Arditi 2006 {published data only}
Axelin 2009 {published data only}
  • Axelin A, Salanterä S, Kirjavainen J, Lehtonen L. Oral glucose and parental holding preferable to opioid in pain management in preterm infants. The Clinical Journal of Pain 2009;25(2):138-45.
Bellieni 2002 {published data only}
  • Bellieni CV, Bagnoli F, Perrone S, Nenci A, Cordelli DM, Fusi M, et al. Effect of multisensory stimulation on analgesia in term neonates: a randomized controlled trial. Pediatric Research 2002;51(4):460-3.
Bellieni 2007 {published data only}
  • Bellieni CV, Cordelli DM, Marchi S, Ceccarelli S, Perrone S, Maffei M, et al. Sensorial saturation for neonatal analgesia. The Clinical Journal of Pain 2007;23(3):219-21.
Campbell-Yeo 2012 {published data only}
  • Campbell-Yeo ML, Johnston CC, Joseph KS, Feeley NL, Chambers CT, Barrington KJ. Cobedding and recovery time after heel lance in preterm twins: results of a randomized trial. Pediatrics 2012;130(3):500-6.
Erlandsson 2007 {published data only}
Ferber 2008 {published data only}
Gabriel 2010 {published data only}
Gazzolo 2000 {published data only}
  • Gazzolo D, Masetti P, Meli M. Kangaroo care improves post-extubation cardiorespiratory parameters in infants after open heart surgery. Acta Paediatrica 2000;89(6):728-9.
Johnson 2007b {published data only}
  • Johnston CC, Filion F, Nuyt AM. Recorded maternal voice for preterm neonates undergoing heel lance. Advances in Neonatal Care 2007;7(5):258-66.
Kashaninia 2008 {published data only}
Miles 2006 {published data only}
Mooncey 1997 {published data only}
  • Mooncey S, Giannakoulopoulos X, Glover V, Acolet D, Modi N. The effect of mother-infant skin-to-skin contact on plasma cortisol and beta-endorphin concentrations in preterm newborns. Infant Behavior & Development 1997;20(4):553-7.
Morelius 2005 {published data only}
  • Mörelius E, Theodorsson E, Nelson N. Salivary cortisol and mood and pain profiles during skin-to-skin care for an unselected group of mothers and infants in neonatal intensive care. Pediatrics 2005;116(5):1105-13.
Reis 2003 {published data only}
  • Reis EC, Roth EK, Syphan JL, Tarbell SE, Holubkov R. Effective pain reduction for multiple immunization injections in young infants. Archives of Pediatrics & Adolescent Medicine 2003;157(11):1115-20.
Schlez 2011 {published data only}
  • Schlez A, Litmanovitz I, Bauer S, Dolfin T, Regev R, Arnon S. Combining kangaroo care and live harp music therapy in the neonatal intensive care unit setting. Israel Medical Association Journal 2011;13(6):254-8.
Silva 2004 {published data only}
  • Silva LM, Clapis MJ. Understanding maternal experiences during her first contact with her child on the birth's room [Compreendendo a vivência materna no primeiro contato com seu filho na sala de parto]. Acta Paulista de Enfermagem 2004;17(3):286-91.
Uga 2008 {published data only}
  • Uga E, Candriella M, Perino A, Alloni V, Angilella G, Trada M, et al. Heel lance in newborn during breastfeeding: an evaluation of analgesic effect of this procedure. Italian Journal of Pediatrics 2008;34(1):3.
Vivancos 2010 {published data only}
  • Zavanella Vivancos RB, Moraes Leite A, Silvan Scochi CG, dos Santos CB. The skin to skin contact at birth and newborn crying during vaccination against Hepatitis B [O contato pele a pele ao nascimento e o choro de recém-nascidos durante vacinação contra Hepatite B]. Acta Paulista de Enfermagem 2010;23(4):461-5.

Additional references

  1. Top of page
  2. AbstractRésumé
  3. Background
  4. Objectives
  5. Methods
  6. Results
  7. Discussion
  8. Authors' conclusions
  9. Acknowledgements
  10. Data and analyses
  11. Contributions of authors
  12. Declarations of interest
  13. Sources of support
  14. Characteristics of studies
  15. References to studies included in this review
  16. References to studies excluded from this review
  17. References to studies awaiting assessment
  18. Additional references
Akman 2002
Anand 2004
  • Anand KJ, Hall RW, Desai N, Shephard B, Bergqvist LL, Young TE, et al. NEOPAIN Trial Investigators Group. Effects of morphine analgesia in ventilated preterm neonates: primary outcomes from the NEOPAIN randomised trial. Lancet 2004;363(9422):1673-82.
Bauer 1998
  • Bauer K, Pyper A, Sperling P, Uhrig C, Versmold H. Effects of gestational and postnatal age on body temperature, oxygen consumption, and activity during early skin-to-skin contact between preterm infants of 25-30-week gestation and their mothers. Pediatric Research 1998;44(2):247-51.
Bohnhorst 2001
Boyle 2004
Campbell-Yeo 2008
  • Campbell-Yeo M, Johnston CC, Filion F, McNaughton K. A comparison of nurse and mother attitudes regarding maternal skin-to-skin care as a pain relieving strategy during heel lance for preterm neonates. 1st European Conference on the Kangaroo Mother Care Proceedings 2008.
Campos 1994
Carbajal 2002
  • Carbajal R, Lenclen R, Gajdos V, Jugie M, Paupe A. Crossover trial of analgesic efficacy of glucose and pacifier in very preterm neonates during subcutaneous injections. Pediatrics 2002;110 (2 Pt 1):389-93.
Carbajal 2005
  • Carbajal R, Lenclen R, Jugie M, Paupe A, Barton BA, Anand KJ. Morphine does not provide adequate analgesia for acute procedural pain among preterm neonates. Pediatrics 2005;115(6):1494-500.
Carbajal 2008
Carfoot 2003
  • Carfoot S, Williamson PR, Dickson R. A systematic review of randomised controlled trials evaluating the effect of mother/baby skin-to-skin care on successful breast feeding. Midwifery 2003;19(2):148-55.
Charpak 2005
Christensson 1992
  • 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 Paediatrica 1992;81(6-7):488-93.
Chwo 2002
  • Chwo MJ, Anderson GC, Good M, Dowling DA, Shiau SH, Chu DM. A randomized controlled trial of early kangaroo care for preterm infants: effects on temperature, weight, behavior, and acuity. Journal of Nursing Research 2002;10(2):129-42.
Cignacco 2007
Conde-Agudelo 2003
  • Conde-Agudelo A, Diaz-Rossello JL, Belizan JM. Kangaroo mother care to reduce morbidity and mortality in low birthweight infants. Cochrane Database of Systematic Reviews 2003, Issue 2. [DOI: 10.1002/14651858.CD002771]
Corff 1995
  • Corff KE, Seideman R, Venkataraman PS, Lutes L, Yates B. Facilitated tucking: a nonpharmacologic comfort measure for pain in preterm neonates. Journal of Obstetric, Gynecologic, and Neonatal Nursing 1995;24(2):143-7.
Craig 1984
Cuzzolin 2001
deLeeuw 1991
  • de Leeuw R, Collin EM, Dunnebier EA, Mirmiran M. Physiologic effects of kangaroo care in very small preterm infants. Biology of the Neonate 1991;59(3):149-55.
Elbourne 2002
  • Elbourne DR, Altman DG, Higgins JP, Curtin F, Worthington HV, Vail A. Meta-analyses involving cross-over trials: methodological issues. International Journal of Epidemiology 2002;31(1):140-9.
Erez 1996
Feldman 2002
  • Feldman R, Weller A, Sirota L, Eidelman AI. Skin-to-skin contact (Kangaroo care) promotes self-regulation in premature infants: sleep-wake cyclicity, arousal modulation, and sustained exploration. Developmental Psychology 2002;38(2):194-207.
Feldman 2003
  • Feldman R, Eidelman AI. Skin-to-skin contact (Kangaroo care) accelerates autonomic and neurobehavioural maturation in preterm infants. Developmental Medicine and Child Neurology 2003;45(4):274-81.
Ferber 2004
  • 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(4):858-65.
Field 2003
  • Field AP. The problem in using fixed-effects models of meta-analysis on real-world data. Understanding Statistics 2003; Vol. 2, issue 2:105-24.
Franck 2001
  • Franck LS, Scurr K, Couture S. Parent views of infant pain and pain management in the neonatal intensive care unit. Newborn and Infant Nursing Reviews 2001;1(2):106-13.
Franck 2002
  • Franck LS, Bernal H, Gale G. Infant holding policies and practices in neonatal units. Neonatal Network - The Journal of Neonatal Nursing 2002;21(2):13-20.
Gibbins 2008
Grunau 2007a
  • Grunau RE, Haley DW, Whitfield MF, Weinberg J, Yu W, Thiessen P. Altered basal cortisol levels at 3, 6, 8 and 18 months in infants born at extremely low gestational age. The Journal of Pediatrics 2007;150(2):151-6.
Grunau 2007b
  • Grunau RE, Tu MT. Long-term consequences of pain in human neonates. In: Anand KJ, Stevens BJ, McGrath PJ editor(s). Pain in Neonates and Infants. 3rd Edition. Philadelphia: Elsevier, 2007:55-76.
Hedges 1998
  • Hedges LV, Vevea JL. Fixed-and random-effects models in meta-analysis. Psychological Methods 1998; Vol. 3, issue 4:486-504.
Holsti 2007
Hummel 2008
  • Hummel P, Puchalski M, Creech SD, Weiss MG. Clinical reliability and validity of the N-PASS: neonatal pain, agitation and sedation scale with prolonged pain. Journal of Perinatology 2008;28(1):55-60.
Hummel 2010
Hunt 2008
  • Hunt F. The importance of kangaroo care on infant oxygen saturation levels and bonding. Journal of Neonatal Nursing 2008;14(2):47-51.
Ibe 2004
  • Ibe OE, Austin T, Sullivan K, Fabanwo O, Disu E, Costello AM. A comparison of kangaroo mother care and conventional incubator care for thermal regulation of infants < 2000 g in Nigeria using continuous ambulatory temperature monitoring. Annals of Tropical Paediatrics 2004;24(3):245-51.
Johnson 2006
  • Johnson AN. The relationship of kangaroo holding to maternal breast milk. Journal of Pediatric Nursing 2006;21(2):137-8.
Johnston 1993
Johnston 1996
Johnston 1997
  • Johnston CC, Collinge JM, Henderson SJ, Anand KJ. A cross-sectional survey of pain and pharmacological analgesia in Canadian neonatal intensive care units. The Clinical Journal of Pain 1997;13(4):308-12.
Johnston 2002
  • Johnston CC, Filion F, Snider L, Majnemer A, Limperopoulos C, Walker CD, et al. Routine sucrose analgesia during the first week of life in neonates younger than 31 weeks' postconceptional age. Pediatrics 2002;110(3):523-8.
Johnston 2007a
Johnston 2007b
  • Johnston CC, Filion F, Nuyt AM. Recorded maternal voice for preterm neonates undergoing heel lance. Advances in Neonatal Care 2007;7(5):258-66.
Johnston 2011b
  • Johnston C, Barrington KJ, Taddio A, Carbajal R, Filion F. Pain in Canadian NICUs: have we improved over the past 12 years?. The Clinical Journal of Pain 2011;27(3):225-32.
Ko 1998
  • Ko Y. Parental stress in the Neonatal Intensive Care Unit (NICU) [Chinese]. Nursing Research (China) 1998;6(5):427-35.
Lagercrantz 1992
Larsson 1996
  • Larsson BA, Norman M, Bjerring P, Egekvist H, Lagercrantz H, Olsson GL. Regional variations in skin perfusion and skin thickness may contribute to varying efficacy of topical, local anaesthetics in neonates. Paediatric Anaesthesia 1996;6(2):107-10.
Lawrence 1993
  • Lawrence J, Alcock D, McGrath P, Kay J, MacMurray SB, Dulberg C. The development of a tool to assess neonatal pain. Neonatal Network 1993;12(6):59-66.
Lefrak 2006
Ludington-Hoe 1992
  • Ludington-Hoe SM, Hashemi MS, Argote LA, Medellin G, Rey H. Selected physiologic measures and behavior during paternal skin contact with Colombian preterm infants. Journal of Developmental Physiology 1992;18(5):223-32.
Ludington-Hoe 1996
  • Ludington-Hoe SM, Swinth JY. Developmental aspects of kangaroo care. Journal of Obstetric, Gynecologic, and Neonatal Nursing 1996;25(8):691-703.
Ludington-Hoe 1999
  • Ludington-Hoe SM, Anderson GC, Simpson S, Hollingsead A, Argote LA, Rey H. Birth-related fatigue in 34-36-week preterm neonates: rapid recovery with very early kangaroo (skin-to-skin) care. Journal of Obstetric, Gynecologic, and Neonatal Nursing 1999;28(1):94-103.
Ludington-Hoe 2004
  • Ludington-Hoe SM, Anderson GC, Swinth JY, Thompson C, Hadeed AJ. Randomized controlled trial of kangaroo care: cardiorespiratory and thermal effects on healthy preterm infants. Neonatal Network - The Journal of Neonatal Nursing 2004;23(3):39-48.
Marsh 1997
  • Marsh DF, Hatch DJ, Fitzgerald M. Opioid systems and the newborn. British Journal of Anaesthesia 1997;79(6):787-95.
McCain 2005
Michelsson 1996
Miles 1989
  • Miles MS, Carter MC, Riddle I, Hennessey J, Eberly TW. The pediatric intensive care unit environment as a source of stress for parents. Maternal-Child Nursing Journal 1989;18(3):199-206.
Miles 1992
Moehn 1996
  • Moehn DG, Rossetti L. The effects of neonatal intensive care on parental emotions and attachment. Infant-Toddler Intervention: The Transdisciplinary Journal 1996;6(3):229-46.
Moore 2007
Oberlander 2000
  • Oberlander TF, Grunau RE, Whitfield MF, Fitzgerald C, Pitfield S, Saul JP. Biobehavioral pain responses in former extremely low birth weight infants at four months' corrected age. Pediatrics 2000;105(1):e6.
Overton 1998
  • Overton RC. A comparison of fixed-effects and mixed (random-effects) models for meta-analysis tests of moderator variable effects. Psychological Methods 1998;3(3):354-79.
Pillai Riddell 2011
Shields-Poe 1997
  • Shields-Poë D, Pinelli J. Variables associated with parental stress in neonatal intensive care units. Neonatal Network - Journal of Neonatal Nursing 1997;16(1):29-37.
Simons 2001
Simons 2003
  • 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. Archives of Pediatrics & Adolescent Medicine 2003;157(11):1058-64.
Stevens 1996
Stevens 1999
  • Stevens B, Johnston C, Taddio A, Jack A, Narciso J, Stremler R, et al. Management of pain from heel lance with lidocaine-prilocaine (EMLA) cream: is it safe and efficacious in preterm infants?. Journal of Developmental & Behavioral Pediatrics 1999;20(4):216-21.
Stevens 1999a
  • Stevens BJ, Johnston C, Franck L, Petryshen P, Jack A, Foster R. The efficacy of developmentally sensitive interventions and sucrose for relieving procedural pain in very low birth weight neonates. Nursing Research 1999;48(1):35-43.
Stevens 2003
Stevens 2007
  • Stevens BJ, Pillai Riddell RR, Oberlander TE, Gibbins S. Assessment of pain in neonates and infants. In: Anand KJ, Stevens BJ, McGrath PJ editor(s). Pain in Neonates and Infants. 3rd Edition. Philadelphia: Elsevier, 2007:67-90.
Stevens 2010a
Stevens 2010b
  • Stevens B, Johnston C, Taddio A, Gibbins S, Yamada J. The premature infant pain profile: evaluation 13 years after development. The Clinical Journal of Pain 2010;26(9):813-30.
van Dijk 2000
  • van Dijk M, de Boer JB, Koot HM, Tibboel D, Passchier J, Duivenvoorden HJ. The reliability and validity of the COMFORT scale as a postoperative pain instrument in 0 to 3-year-old infants. Pain 2000;84(2-3):367-77.
Warnock 2010
  • Warnock FF, Castral TC, Brant R, Sekilian M, Leite AM, Owens Sde L, et al. Brief Report: Maternal kangaroo care for neonatal pain relief: A systematic narrative review. Journal of Pediatric Psychology 2010;35(9):975-84.
Wereszczak 1997
  • Wereszczak J, Miles MS, Holditch-Davis D. Maternal recall of the neonatal intensive care unit. Neonatal Network - Journal of Neonatal Nursing 1997;16(4):33-40.
Whitelaw 1985
  • Whitelaw A, Sleath K. Myth of the marsupial mother: Home care of the very low birth weight babies in Bogota, Colombia. Lancet 1985;1(8439):1206-8.
Yamanda 2008
  • Yamanda J, Stinson J, Lamba J, Dickson A, McGrath PJ, Stevens B. A review of systematic reviews on pain interventions in hospitalized infants. Pain Research & Management 2008;13(5):413-20.
Youngblut 1992
  • Youngblut JM, Shiao SY. Characteristics of a child's critical illness and parents' reactions: preliminary report of a pilot study. American Journal of Critical Care. 1992;1(3):80-4.