The nine stages of skin‐to‐skin: practical guidelines and insights from four countries

Abstract Incorporating systematic evidence with clinical expertise is a key element in the quest to improve quality of care and patient outcomes. The evidence supporting skin‐to‐skin contact in the first hour after birth is robust and includes significantly improved outcomes for both mother and infant. This paper compares available iterative data about newborn behaviour in the first hour after birth to further describe the observable behaviour pattern and to provide clinical insight for further research. Although the evidence for positive outcomes through skin‐to‐skin contact are robust, there is a dearth of research specifically focused on clinical practice. The methodology considers the four available data sets that used Widström's 9 stages, which consists of studies from Japan, Sweden, Italy and the United States, examining the parameters of each stage across settings from around the world. This research provides an expanded understanding of the timing of the newborn's progression through Widström's 9 observable stages. We found that newborns in all four data sets began with a birth cry and continued through the remaining stages of relaxation, awakening, activity, rest, crawling, familiarization, suckling and sleeping during the first hours after birth and consolidated the data into a Sign of the Stages chart to assist in further research. The evidence supports making a safe space and time for this important newborn behaviour. Clinical practices should encourage and protect this sensitive period.

Despite the research and compelling directives from world authorities, the implementation of immediate, continuous and uninterrupted SSC for all healthy mothers and newborns, regardless of feeding choice, has not become standard practice. According to UNICEF, only 45% of newborns experienced early SSC and breastfeeding (UNICEF, 2016 However, the question asked is 'How many patients experience mother-infant skin-to-skin contact for at least 30 min within 1 h of uncomplicated vaginal birth?' or 'How many patients experience mother-infant skin-to-skin contact for at least 30 min within 2 h of uncomplicated caesarean birth?' This does not meet the definition of immediate, continuous and uninterrupted SSC as described by WHO or UNICEF. Indeed, the most recent Cochrane review of early SSC for mothers and their healthy newborn infants highlights the inconsistencies of practice throughout the published research, reflecting the inconsistencies in clinical practice throughout the United States and the world. Only 47% of the eligible trials reported 'early' or 'immediate' SSC. The duration was inconsistent as well, from 15 min to 30 h (Moore et al., 2016).
Skin-to-skin care, on the other hand, implies a process, consistent with immediate, uninterupted contact between the mother and baby for an hour or more after the birth, during which maternal and infant assessments are incorporated, and the newborn goes through nine observable stages. These stages were first described by Widström (A. M. Widström et al., 1987) and later illustrated with a video (Widström, Ransjö-Arvidsson, & Christiansson, 2010), two expanded papers Widström, Brimdyr, Svensson, Cadwell, & Nissen, 2019) and a video directed at staff implementation (Brimdyr, Widström, & Svensson, 2011): Birth Cry, Relaxation, Awakening, Activity, Crawling, Resting, Familiarization, Suckling and Sleeping ( Figure 1) during the first hour after birth (Brimdyr et al., 2011;Widström et al., 2010;Widström et al., 2011;Widström et al., 2019). The nine stages recognize the work of the mother and baby during this time, the complex system of hormones, instinctive behaviours and bonding, which goes beyond the implied passivity of simply putting the newborn skin-to-skin for a short time. There is work, and competent behaviours, that occur during this vital and unique time. Skin-to-skin care supports a newborn's exploration and self-attachment, a result of the newborn's instinctive survival behaviour to find the breast and start suckling within an hour or so of the birth, leading to increased breastfeeding at discharge (Bramson et al., 2010), increased breastfeeding self-efficacy (Aghdas, Talat, & Sepideh, 2014) and more optimal latch (Righard & Alade, 1992) and bypasses the issues associated with 'hands-on' or forced latch (Svensson, Velandia, Matthiesen, Welles-Nyström, & Widström, 2013).
Although the research and evidence are robust, there is a dearth of iterative research specifically focused on clinical practice. Recently, implementation of clinical practice was clarified to address the lag between research knowledge and clinical practice, to translate existing knowledge and guide clinician behaviour change (Widström et al., 2019). This paper contributes to the field by examining the worldwide similarities of newborn behaviour when skin-to-skin immediately after birth and defines the expectations and parameters of each of Widström's 9 stages in order to provide a practical guideline for clinicians and researchers.

| METHODS
In this manuscript, previously published data on the observable behaviours of the newborn during the first hour after birth when placed skin-to-skin with mother immediately after birth were

Key messages
• This paper considers the data about newborn behaviour in the first hour after birth from four countries, Sweden, Italy, Japan and the United States, to further describe the distinctive and observable behaviour pattern in order to assist clinicians and researchers to recognize the expectations and parameters of each of the nine stages.
• The behaviour of the newborn infant while skin-to-skin during the first hour or so after birth varies little from one practice setting to another.
• Clinical practices should encourage and protect this unique and important time by ensuring adherence to Step 4 of the BFHI, including immediate, continuous and uninterrupted skin-to-skin contact between all mothers and newborn infants during the first hour after birth.
compared between different groups of infants, and median and quartiles were used, if available. Some videos from the United States and Japan were reanalysed by research assistants.
A literature review found only four studies (Brimdyr, Cadwell, Stevens, & Takahashi, 2017;Brimdyr et al., 2015;Dani et al., 2015; from Japan, the United States, Italy and Sweden, respectively, which have reported on the nine stages of newborn behaviour in relation to healthy newborn babies, born vaginally. Each hospital followed the World Health Organization guidelines for SSC between mother and newborn. Ethical permission for each study is reported in the original papers. Widström et al. report on a convenience sample of 28 clinically uncomplicated vaginal birth Swedish newborns, many of whom were exposed to meperidine, epidural, pudendal block and so forth in labour . The median and quartiles are pub- The data used in this paper from the Swedish and Italian studies have been published elsewhere (Dani et al., 2015;Widström et al., 2011). New data are presented from the United States and Japanese studies (Brimdyr et al., 2017(Brimdyr et al., , 2015. Existing videos were reanalysed in relation to the newly developed Sign of the Stage chart (Table 1). Education of the research assistants was conducted using a professional video (Brimdyr et al., 2011) and a workshop about Widström's 9 stages of newborn behaviour to ensure recognition of each stage. MAXQDA 11.0.2, 2013, a professional qualitative data analysis software, was used to separately and independently code the video recordings for Widström's 9 stages. Any inconsistencies required review and consensus. The Japanese videos and American videos were recoded to focus on the initial entry into each stage. The data were then charted onto the Sign of the Stage chart (Table 1), which could be used to generate the median and quartile data (Table 2).

| RESULTS
The number of babies reported in each behaviour phase in the studies from the United States, Japan, Italy and Sweden are documented in Table 2. All of the newborns experienced a Birth Cry. All of the T A B L E 1 Nine stages for clinical practice: A chart to aid in the understanding of when a stage begins during skin-to-skin contact with mother and summary of maximum and minimum quartiles from four studies Widström Table 3, which reflects the data reported by each study.

| DISCUSSION
All of the newborns reported on in the United States, Japan, Italy and Sweden experienced some version of a Birth Cry. Despite its name, the Birth Cry Stage is about more than just noise. It is the time when the newborn's lungs expand, transitioning from in-utero reliance on the placenta for oxygen to a time of breathing air. Although this is traditionally noticed through a noisy cry, the transition to breathing air can sometimes be marked only through an inhalation or a small cough.
This stage could also be marked by other newborn behaviours, including a startle reflex, a sudden opening of the eyes and grasping of the umbilical cord. However, its defining behaviour is the expansion of the lungs and breathing air. The Birth Cry produces a wealth of information about the baby's condition (Branco, Behlau, & Rehder, 2005) and is considered as part of the APGAR score.
The majority of staff interaction with the newborn occurs during this stage. During the period of the Birth Cry, the newborn is dried and placed gently on the semireclined mother's chest. The newborn T A B L E 2 Number of babies reported in each behavioural phase during skin-to-skin contact in the United States, Japan, Italy and Sweden studies United States (n = 11) Japan (n = 13) Italy (n = 17) Sweden (n = 28)

T A B L E 3
Median time at appearance (minutes) from birth of behavioural stage during skin-to-skin contact and interquartile range (25th-75th quartile)

Stage/country
United States (n = 11) Japan (n = 18) Italy (n = 17) Sweden *(n = 28) Birth Cry 0 (0-0) 0 (0-0) 0 (0-0) 0 (0-0) should be prone, with hands on either side of the body and head turned to the side, to maximize skin contact and warmth. The staff must use gentle hands in order to not hinder the expansion of the newborn's lungs. The umbilical cord is usually long enough to allow the newborn to be placed skin-to-skin with the mother without cutting the cord prematurely. After the newborn is settled with the mother, the majority of staff interaction throughout the following hour or so involve monitoring and assessing the newborn, which can occur while the newborn remains skin-to-skin with the mother.
In the first minutes after the birth, all but 8 of the 69 newborns in this reanalysis experienced a period of Relaxation. The Relaxation Stage begins after the newborn is settled on the mother's chest. At this point, the newborn stops crying and lays still. This behaviour may be the 'fear-induced freezing' , which occurs during a perceived threat or a 'startle-induced behavioural arrest', which occurs prior to a cognitive assessment of a new situation (Roseberry & Kreitzer, 2017). If The newborn will self-attach and suckle around 50 min after the birth. During this first experience of suckling, the 'usual rules' of breastfeeding-nose to nipple, gape, asymmetric latch-do not apply.
The newborn's latch will be appropriate for this early learning experience of suckling colostrum. The newborn may begin to make soliciting sounds, lick, suckle and then adjust the mouth-to-nipple contact several times to optimize the suckling position. The newborns in the United States, Japan and Italy data are unmedicated and self-attach at a median of 52, 52 and 45 min. It is interesting to note that the Swedish newborns self-attach around 62 min, which may be associated with the labour medication exposure of those infants (Brimdyr et al., 2015;Nissen et al., 1997;Ransjö-Arvidson et al., 2001).

| Limitations
This study is limited to the four studies which reported on the nine stages in relation to healthy newborn babies, born vaginally. Although the ward routines were not standardized, the reported differences in newborn behaviour was very small. Additionally, the United States study and the Japanese study only recorded the first hour after birth, which means that behaviours that occurred after the first 60 min were not recorded or included. In addition, the Swedish study included 10 mothers who had been exposed to meperidine (Pethidine hudrochloride, ACO Pharmacia).
A limitation of this study is that the majority of Japanese videos followed their interpretation of the older World Health Organization definition of Step 4, which invited staff to 'Help mothers initiate breastfeeding within a half hour of birth' (World Health Organization & UNICEF, 1989), and therefore, innate newborn behaviour was not observed after 30 min, since newborns had been 'helped' to initiate breastfeeding.
Both the Japanese and American data were scored on the chart (Table 2); it is assumed that the others used similar specifications, although that is not known. However, Table 2 is based on the work of the Swedish research cited here. We also postulate that the Italian research was based on this Swedish work. Therefore, all methods of analysis are based on initial reports of the nine stages in Widström's seminal work , which has recently been enhanced and strengthened (Widström et al., 2019). Despite this unknown, the similarity of timing is noteworthy.

| CONCLUSION
The comparison of four data sets from around the world-Japan, Swe-