Tactile stimulation in low-risk infants: Results of a systematic Review Angela Underdown Associate Professor in Early Childhood, University of Warwick Jane Barlow Associate Professor, Reader in Public Health, University of Warwick Address for Correspondence: Angela Underdown Warwick Medical School University of Warwick Coventry CV4 7AL Tel: 02476 574884 Email: A.V.Underdown@warwick.ac.uk Key words: tactile stimulation, infants, systematic review Tactile stimulation in low-risk infants: Results of a systematic Review Abstract Touch, an intrinsic part of caring for an infant, establishes powerful physical and emotional connections, and plays an important role in supporting health and wellbeing, and in particular affect regulation. The objective of this study was to investigate published research to ascertain whether tactile stimulation offers an effective intervention to support infant mental and physical health. A systematic review into the effects of infant massage on low-risk infants under 6 months identified twenty-two studies (13 from China and 9 from elsewhere) that met our inclusion criteria. Study criteria allowed only for randomised controlled trials to be included. Study quality was variable. Beneficial effects for mother-infant interaction, maternal warmth and reduction of intrusiveness, infant attentiveness, liveliness and happiness were demonstrated in one study; other studies reported no beneficial effect on infant temperament, attachment or development. Individual studies reported beneficial effects on amount of crying, serum levels of norepinephrine and epinephrine, and nocturnal urinary secretion of 6sulphatoxymelatonine and urinary cortisol. Beneficial effects on patterns and quality of sleep were reported in two studies, and on length of sleep in studies from China but not elsewhere in the world. Effects on weight, length and head circumference were evident only in the meta-analysis of studies from China, and in a large study from a Korean orphanage in which normal infant care was highly atypical. It is concluded that there is some evidence that infant massage may have beneficial effects on infants’ sleep and crying patterns, mother-infant interaction and the infant’s physiological response to stress. There is also some evidence that infant massage may be beneficial for infant growth, specifically in situations where infants are deprived of sufficient adult contact, but all of these findings require more robust studies. No evidence was presented that infant massage does harm. 2 Tactile stimulation in low-risk infants: Results of a systematic Review Introduction Touch is an intrinsic part of caring for an infant that establishes powerful physical and emotional connections between carer and baby, and plays a pervasive role in communication and affect regulation (Moszkowski and Stack 2007). For most infants, everyday routines involve many tactile interactions, communicating a range of somatosensory messages including emotional feelings, pressure, temperature, texture, softness or even pain. The amount of touch considered appropriate between adults and infants varies between cultures with some babies experiencing close contact with the mother’s body during most of the first year while others experience extended periods of separation by being encouraged to sleep alone in the nursery and through the use of day-care (Rogoff 2003). Maternal sensitivity has been identified as a significant component in the development of an infant’s emotional attachment (Ainsworth 1973), and the sensitivity (or otherwise) of a carers’ responses is transmitted to the infant through a combination of touch, voice and facial movements. During the past decade there has been increasing recognition about the specific role of touch or tactile stimulation in the development of the infant’s capacity for affect regulation. Affect Regulation and the Role of Touch The formation of psychological attachments appears to be interlinked with chemical changes and functional development in the infant neural system (Schore 2003), and sensitive tactile stimulation during maternal nursing of the infant, is thought to play a significant role in the growth of the dendrites that form the crucial neural connections (Greenough and Black 1992 cited in Schore 2003). In primates, neurobiological research has shown that ‘critical levels of tactile input of specific quality and emotional content is important for normal brain maturation’ (Martin et al 1991:3355). At birth the primary somatosensory centre, 3 which processes tactile and kinesthetic information in the brain’s cerebral hemispheres, is metabolically active (Chugani 1996). The hypothalamicpituitary-adrenocorticol (HPA) system produces and regulates the glucocorticoid cortisol in response to stress (Gunnar 1998) and for the first two months after birth the infant’s HPA system is highly labile (Gunnar, Brodersen, Krueger and Rigatuso 1996). However, from the age of about two months the infant’s stress systems are becoming organised via transactions with the sensitive main carer who acts as a ‘buffer’ to the reactivity of the HPA system (Nelson and Bosquet 2000). Touch has been reported as an intrinsic factor in helping to regulate infant behavioural states (Brazelton 1990) and de Chateau (1976) found that infants who had extra bodily contact after birth smiled more and cried less at three months observation. By 8 weeks post-natally the somatosensory connections to the amygdala (the almond shaped group of neurons located deep within the brain’s temporal lobes that have a major role in the processing and memory of emotional reactions) are forming and Schore (2003) suggests that sufficient levels of tactile stimulation releases early pro-attachment behaviour. It is the security that most children experience within their attachment relationships that is thought to impact upon the high neonatal cortisol responses, so that by the age of one year infants are less likely to show an increase in response to stressors (Gunnar and Donzella 2002). This appears to be due to the development of functional glucocortoid hyporesponsiveness, as children learn to feel secure and safe with caregivers who respond to their cues (Gunnar and Donzella 2002). However, Gunnar and Donzella (2002) further report that elevated cortisol levels have been noted when children are exposed to moderately less sensitive and responsive care. These findings are supported by ethological studies (Liu et al 1997) which have demonstrated that the amount of tactile stimulation (maternal licking and grooming) experienced by rodent pups 4 modulates cortisol production. Harlow’s famous studies also demonstrated the importance of tactile experience by replacing the rhesus monkey mothers with wire mesh dummies, one dispensing milk from a bottle and the other clad in terry toweling cloth (Harlow 1958). The monkeys clung to the tactile surrogate mother when fearful and were more confident to explore when it was present (Harlow 1958). In other studies Harlow (1965; 1971) demonstrated that isolated monkeys developed abnormal social behaviour and later failed to care for their young. Other studies (Mitchell 1970; Goosen 1981; Kraemer 1985) have produced similar findings of abnormal social and motor behaviour in socially deprived monkeys. More recent work (Martin et al 1991) investigating the neurobiological mechanisms underlying the behaviour of socially deprived monkeys found that social/sensory deprivation of non-human primates in the first year of life have pronounced alterations in the organization and patterned arrangements of the basal ganglia neurotransmitters. The basal ganglia are a group of subcortical nuclei involved in motor control, cognition, and emotion (Carver and Carver 2003) and abnormalities in this region are characterised by abnormal movements and a number of neuropsychiatric disorders (Carver and Carver 2003). Evidence from neurobiological research on primates therefore suggests that “in early postnatal life, maintenance of critical levels of tactile input of specific quality and emotional content is important for normal brain maturation” (Martin 1991:3355). Research with human infants has been restricted to naturally occurring situations where children have been raised in highly adverse conditions. Children living in Romanian orphanages, who lacked social and physical stimulation and opportunities to form emotional attachments with consistent care-givers had complex ‘flattened’ cortisol profiles that did not show the expected daily rhythm, with raised levels in the morning (Carlson et al 1995; Carlson et Earls 1997). This finding suggests that HPA axis activity may have been adversely affected (Gunnar and Vazquez 2001), and although no firm conclusions were possible from this data (Gunnar and Donzella 2002), other evidence shows that children 5 raised in orphanages of this type have stunted growth (Johnson 2000). Elevated corticotrophin-releasing hormones (CRH) are thought to be instrumental in this type of faltering growth (Johnson et al 1992). Intervening using tactile stimulation Tactile stimulation or infant massage is widely practiced in many parts of the world, especially Africa, Asia and the South Pacific (Field, Schanberg, Davalos, Malphurs 1996). A survey of 332 primary caretakers of neonates in Bangladesh, for example, found that 96% engaged in massage of the infant's whole body between one and three times daily (Darmstadt et al 2002). In the West, tactile stimulation has until recently been largely restricted to highrisk infants often in intensive care settings, in which the amount of handling that an infant received was thought to be suboptimal (Field 2000 cited in Zeanah 2000; Vickers 2000). Increasingly, however, parents in western cultures are being taught the techniques of tactile stimulation or infant massage (Underdown cited in Barlow and Svanberg in press) often by attending a weekly class. Claims for the effects of such stimulation are wide and include benefits for parent-infant interaction, sleep, respiration, elimination and the reduction of colic and wind (Blackwell 2000; Field 2000 cited in Zeanah 2000). The aim of this review was to address whether tactile stimulation in medically low-risk infants could be shown to have an impact on either the mental well-being of infants or the relationship between the mother and the baby. Data on infant growth has also been included, due to the complexity of the relationship between growth and other aspects of mental health. Method A systematic review of randomised controlled trials was conducted. Searches were undertaken of a range of electronic databases including CENTRAL 2005 (Issue 3), MEDLINE (1970 to 2005), PsycINFO (1970 to 2005), CINAHL (1982 to 2005), EMBASE (1980 to 2005), and a number of other Western and Chinese 6 databases. We only included studies that had examined the impact of any form of tactile stimulation on low-risk infants under the age of six months. The intervention was defined as ‘systematic tactile stimulation by human hands’ (Vickers 2004) and low-risk infants were defined as having no apparent physical health adversities. Studies comprising infants of post-natally depressed mothers (Field et al 1996; Onozawa et al 2001) and those being cared for in an orphanage (Kim et 2003) were included (i.e. as they were reported on healthy full-term infants, whereas infants who were HIV exposed (Scafidi et al 1996) were excluded. Studies were included if infants were randomised to either a tactile stimulation group or a control group that received no intervention or standard care. No language restrictions were applied. Data management Data were extracted, checked and entered into RevMan version 4.2 (Cochrane Collaboration, 2003) by two reviewers independently. Discrepancies were discussed with a third reviewer. Assessment of quality and risk of bias Trials were assigned a quality category based on allocation concealment. Aspects of study design that may increase bias were also appraised (sample size, number of infants lost to follow-up, the method of dealing with attrition/drop out, use of blinding to assess outcomes, and whether there was any assessment of the distribution of confounders). Data synthesis Using a random effect model we report the differences in continuous outcomes between the treatment and control groups as weighted mean differences with 95% confidence interval. In the case of measures where data were reported on incompatible scales, we present the standardised mean difference and 95% confidence intervals. Where it was not possible to synthesise the data, effect 7 sizes and 95% confidence intervals have been calculated for individual outcomes in each study. In the absence of data with which to calculate effect sizes we report the significance level presented in the primary study. A minus sign indicates a result favouring the intervention group. Due to concerns about uniformly positive results, inadequate information about the design and conduct, and the absence of any reported dropout, a post hoc decision was taken to analyse separately the results of thirteen studies undertaken in China (Liu Chun Li 2005; Liu 2005; Lu Jiao, Li Ju Zhan, Wu Li Fang 2005; Na Zhuo Hua, Xie Hui Yun, Huang Jian Hua 2005; Shao L et al.2005; Sun Hai Yun, Gao Xiang Yu, Zhao Xue Mei 2005; Ye Hong Yun 2004; Xua Li Shuan, Qing Gui Romg, Ye Mei Yan et al 2004; Duan Lihong, Li Weihong, Shi Fentao 2002; Shi Li, Xue, Rong 2002; Ke, Ling, Li. 2001; Zhai, Pan Xian, Hua et al 2001; Wang Bin, Shen Yue Hua, Jin Run Yan et al 1999). Sensitivity Analysis A sensitivity analysis was undertaken to assess the impact on the findings of one large Korean study (Kim, Shin, White-Traut 2003) of infants receiving orphanage care. Results We identified 809 abstracts in Western databases, of which 35 were obtained for review. Ten studies met the inclusion criteria, one (Koniak Griffin, Ludington-Hoe et al 2001) of which reported follow-up of one of the other nine and one of which was carried out in China (Duan Lihong, Li Weihong, Shi Fentao 2002). A handsearch of references resulted in the identification of one further study (Ke, Ling, Li 2001). Of the abstracts reviewed from the Chinese databases,12 studies were identified as suitable for inclusion, producing in total 13 Chinese studies (Liu Chun Li 2005; Liu 2005; Lu Jiao, Li Ju Zhan, Wu Li Fang 2005; Na Zhuo Hua, Xie Hui Yun, 8 Huang Jian Hua 2005; Shao L et al.2005; Sun Hai Yun, Gao Xiang Yu, Zhao Xue Mei 2005; Ye Hong Yun 2004; Xua Li Shuan, Qing Gui Romg, Ye Mei Yan et al 2004; Duan Lihong, Li Weihong, Shi Fentao 2002; Shi Li, Xue, Rong 2002; Ke, Ling, Li. 2001; Zhai, Pan Xian, Hua et al 2001; Wang Bin, Shen Yue Hua, Jin Run Yan et al 1999) In addition to the Chinese studies, one Korean (Kim, Shin, White-Traut 2003), one Israeli (Goldstein Ferber et al 2002), one British (Onozawa, Glover et al 2001) one Indian (Argawal, Ashish et al 2000), and five North American (Elliot, Reilly 2002; Cigales, Field et al 1996; Jump 1998; Field, Grizzle et al 1996; Koniak Griffin, Ludington-Hoe 1988) studies were included. One follow-up study was also included (Koniak Griffin, Ludington-Hoe et al 1995). Table one shows the characteristics of the included studies. Table 1 Types of studies A range of tactile stimulation or massage methods were reviewed. In four studies (Argawal 2000; Elliott 2002; Goldstein Ferber 2002; Koniak-Griffin 1988) parents were taught massage techniques prior to them conducting massage on their infants in the home. In two studies massage was offered by research associates (Cigales 1997; Field 1996). In the Kim (2003) study, orphans received a multimodal intervention of massage, talking and eye contact from research associates who were trained to be responsive to the infants’ responses. Although it was not possible to isolate the effects of eye contact and talking, this study was included because both these components are an intrinsic part of some included infant massage programmes. In the 13 Chinese studies the massage was mostly administered by a nurse with specialist training in infant massage, following which the technique was taught to the parents who continued the massage at home. 9 Types of massage The massage programmes evaluated in the included studies varied in terms of duration and frequency. In one study, infants received a daily 30 minutes intervention over 14 days (Goldstein Ferber 2002). In the Kim (2003) study infants were massaged 15 minutes, twice daily for 4 weeks. In further studies, infants received 10 minutes of massage daily over a four week period (Argawal 2000) or a minimum of 10 minutes massage daily over 16 weeks (Elliott 2002). In the Field (1996) study infants received 15 minutes of massage twice weekly over a period of six weeks and in the Koniak-Griffin (1988) study infants received 5-7 minutes of massage daily over 3 months. In two studies (Jump 1998 and Onozawa 2001) mothers were taught massage techniques for approximately an hour per week as part of four, weekly, group-based sessions, following which the continuation of this practice at home varied according to parental motivation. In the 13 Chinese studies infants were mostly massaged for fifteen minute periods up to three times a day over a period extending up to 6 weeks (Liu 2005; Liu Chun 2005; Lu 2005; Na 2005; Shao 2005; Sun 2004; Ye 2004; Xua 2004; Duan 2002; Shi 2002; Ke 2001; Zhai 2001; Wang 1999). In the Cigales study (1997) massage was administered only once prior to the conducting of an experimental task to assess the impact of massage on cognitions. Findings Stress hormones One US study (Field et al 1996) showed reduced levels of norepinephrine (weighted mean difference -60.30 ng/gm creatinine 95% confidence intervals 111.88 to -8.72) and epinephrine (weighted mean difference -13.00 ng/gm creatinine 95% confidence intervals -20.08 to -5.29) among massaged infants, but no effect on levels of serotonin (weighted mean difference -295.50 ng/gm creatinine 95% confidence interval -705.25 to 114.25). This study also measured salivary cortisol levels 20-minutes post-intervention and showed no difference between groups (weighted mean difference -0.20 ng/dl 95% confidence interval 10 -4.60 to 4.20) (Field et al 1996). However, urinary cortisol levels measured later using radioimmune assay, were lower in the massage group (weighted mean difference -360.40 ng/gm creatinine 95% confidence intervals -633.79 to -87.01). Circadian Rhythms An Israeli study (Goldstein Ferber et al 2001) measured the nocturnal secretion of 6-sulphatoxyymelatonin in urine and showed higher levels in the massaged group (weighted mean difference -523.03 ng/night 95% confidence interval 664.51 to -381.55), suggesting that massage enhances circadian rhythms by promoting the secretion of melatonin. Infant sleep/wake behaviours The above study also showed at 8-weeks postnatal peak activity during the time period 3 - 7 a.m. in the massaged group compared with 11 p.m. - 3 a.m. in the control group. A secondary peak of activity was observed in the treated subjects between 3 p.m. and 7 p.m. while in the control group a secondary peak occurred between 11 a.m. to 3 p.m. This suggests a delay in peak activity in massaged infants and that the treated infants achieved a more favourable adjustment of their rest-activity cycle. An interaction between treatment and timing of peak activity was observed (p=0.042). No differences were found between groups in total movement. No differences were found for measurements performed 1-day before and 1-day after the intervention, and at 6-weeks of age. One US study (Field et al 1996) showed less crying (weighted mean difference 8.20 episodes 95% confidence interval -12.24 to -4.16) and increased active sleep in the massaged group (weighted mean difference -37.00 95% confidence interval -50.86 to -23.14). Infants in the control group spent more time in an inactive alert state 12.70 (6.02 to 19.38). A non-significant increase in measures of quiet sleep 6.30 (-7.56 to 20.16) was also observed in this group. There was no difference between massage and control groups in the amount of drowsiness 11 -2.00 (-4.19 to 0.19) (Field et al 1996). One further study that assessed duration of sleep and number of naps after four weeks of massage showed no difference between the two groups (Argawal et al 2002). One of the Chinese studies (Xua, Shuan et al 2003) measured the frequency and duration of bouts of crying and found the massaged group to have fewer bouts of crying -0.34 (-0.56 to -0.12) that lasted for shorter periods of time (hrs) -0.30 (0.54 to -0.06). Three of the thirteen Chinese studies (Zhai, Pan et al 2001; Sun etal 2004; Xua el al 2004) including 434 infants (216 intervention and 218 in the control group) measured hours of sleep. Meta-analysis showed massaged infants to sleep longer -0.62 hrs (-1.12 to -0.12). One Chinese study (Xua el al 2004) also measured the frequency and duration of night waking and found the massaged group woke fewer times -0.48 (-0.81 to 0.15) for significantly shorter periods -0.27hrs (-0.51 to -0.03) Infant Interactions A British study (Onozawa, Glover et al 2001) showed improvements in the intervention group for three aspects of infant interaction including attentiveness (standardised mean difference -1.31 95% confidence interval -2.26 to -0.37); liveliness (standardised mean difference -1.30 95% confidence interval -2.24 to 0.36) and happiness (standardised mean difference -0.95 95% confidence interval -1.85 to -0.06). This study also showed an impact on mother-infant interaction using an independent assessment of outcome (standardised mean difference -1.32 95% confidence interval -2.27 to -0.38). Differences favouring the intervention group were also observed for the amount of warmth (standardised mean difference 2.17 95% confidence interval -3.27 to -1.07) and intrusiveness (standardised 12 mean difference -0.97 95% confidence interval -1.87 to -0.08) of maternal interactions in the massage group. Growth Meta-analysis of the effects of massage on infant weight was undertaken based on findings from four non-Chinese studies (Kim et al 2003; Argawal et al 2000; Field et al 1996; Koniak Griffin et al 1988). Based on a total sample of 264 infants the results showed a large but non-significant increase in infant weight (297.72 gms 95% confidence interval 859.26 to 263.81]. Figure 1 Meta-analysis of weight gain This finding was heavily dependent on the data from a large study of Korean orphanage infants (Kim et al 2003) and a sensitivity analysis was therefore undertaken in which the data from this study were removed from the metaanalysis. The exclusion of this study resulted in a reduction in the weighted mean difference to 4.12 gms (95% confidence interval 223.91 to 232.16). Figure 2 Sensitivity analysis for weight Ten of the 13 Chinese studies (Liu Chun Li 2005; Liu 2005; Lu Jiao et al 2005; Na et al 2005; Sun et al 2005; Ye et al 2004; Duan et al 2002; Shi et al 2002; Ke, et al 2001; Zhai 2001) evaluated the effectiveness of infant massage on weight gain (based on results from 1570 infants); meta-analysis showed a significant increase favouring the intervention group -378.12 (-511.02 to -245.22). Figure 3 Meta-analysis of weight Chinese Studies Two non-Chinese studies evaluated the impact of massage on infant length (Kim et al 2003; Argawal et al 2000). They comprise a sample of 183 infants; meta- 13 analysis showed no impact (weighted mean difference 0.76 cms 95% confidence interval -2.67 to 1.15). Figure 4 Meta-analysis of length Six of the thirteen Chinese studies (Liu 2005; Lu Jiao et al 2005; Na et al 2005; Duan et al 2002; Shi et al 2002;) comprising a total of 1120 infants measured infant length; meta-analysis showed massaged infants to be longer (cms) -0.93 (1.21 to -0.64). Figure 5 Meta-analysis of length Chinese Studies Two non-Chinese studies comprising 183 infants evaluated the impact of massage on infant head circumference (Kim et al 2003; Argawal et al 2000). Meta-analysis showed no impact (weighted mean difference -0.87 cms 95% confidence interval -2.62 to 0.87). Figure 6 Meta-analysis of head circumference Five of the thirteen Chinese studies (Liu 2005; Lu Jiao et al 2005; Na et al 2005; Duan et al 2002; Ke, et al 2001) including 1040 infants measured infant head circumference and meta-analysis showed a benefit of 1.48 cms(-1.70 to -1.26) in massaged infants. Figure 7 Meta-analysis of head circumference Chinese Studies Number of illnesses and clinic visits Massaged Korean orphanage infants had fewer illnesses (weighted mean difference -8.82 95% confidence interval -10.41 to -7.23) and clinic visits (weighted mean difference -5.98 95% confidence interval -6.94 to -5.02) than controls (Kim et al 2003). 14 Other outcomes One USA study showed an effect on habituation (Cigales et al 1997) but there was no evidence in other USA studies of benefit on a range of measures of infant temperament, (Elliot et al 2002; Jump 1998; Field et al 1996) infant attachment,(Jump 1998) or psychomotor and mental development (Koniak Griffin et 1995). Discussion The methodological quality of the included studies was variable, and has been reported elsewhere (Underdown et al 2006). The largest number of studies were conducted in China and they show significant effects on weight, length and head circumference. Based on concerns about Chinese studies raised previously (Vickers et al 1997) that were also apparent in these studies (uniformly significant results, inadequate information about the design and conduct of the studies, and absence of any reported dropout), we took the decision to present the results of the Chinese studies in a separate meta-analysis. These studies examined the effect of very similar amounts and durations of massage (i.e. fifteen minutes, twice daily over around six weeks), but considerable statistical heterogeneity was noted, even after taking account of the individual results and the sample sizes. The reason for this is not clear. The results of these studies must therefore be viewed with considerable caution. The quality of the remaining studies was only fair with many not providing specific details about the method of randomisation or about allocation concealment. There was also some heterogeneity in the infant massage interventions. For example, in some studies the massage was administered by the mother, while in others it was administered by researchers/professionals. The duration and frequency of massage also varied from one episode for 8 minutes to 15 minutes three times a day for 6 weeks. Although specific detail was often not provided, it would appear that the approach to massage also varied 15 including the use of tactile and kinaesthetic stimulation in one and responsiveness to infant cues in another. Synthesis of data was undertaken using a random effect model despite this variation because we were not aware of any evidence to indicate that any of these factors are influential in altering outcomes. This variation, however, makes it very difficult to identify the core components of effective massage intervention. Bearing these limitations in mind, the evidence of significance effects of massage on catecholamine (norepinephrine and epinephrine) and cortisol excretion are potentially important given what we now know about the possible damaging effects of stress hormones on the development of pathways in the infant brain (Gunnar et al 1998 cited in: Zeanah 2000). Given the apparent effect of infant massage on stress hormones it is not surprising to find some evidence of an effect on sleep and crying and one study (Goldstein Ferber 2002) also reported an effect on release of melatonin (6-sulphatoxymelatonin), which is involved in the adjustment of circadian rhythms. As sleep deprivation is a very real problem for many families with a young infant, the teaching of infant massage may be an effective practical way of helping parents to support infants in establishing sleeping patterns. Meta-analyses of growth in weight, length and head circumference in the nonChinese studies showed non-significant differences favouring the intervention group that disappeared following a sensitivity analysis in which the results of the large Korean study of orphanage infants were removed. The highly significant findings of the Korean study may have been due to severe deprivation of tactile stimulation in the orphanage control group infants. Certainly there is research to show that infants who are deprived of touch, such as those in orphanages with low infant-adult ratios, do not achieve optimum growth (Mason and Narad 2005). Field (1996) found a non-significant weight gain favouring the intervention group of infants of depressed mothers. However, this study used researchers to 16 massage infants, which raises questions about the promotion of attachment in combination with sensitive touch (Schore 2003). Ten of the 13 Chinese studies reported a significant increase in weight following infant massage, although as noted earlier more information is needed about these studies before any conclusions can be drawn. There is a need for further studies to identify whether learning infant massage may be an effective intervention in some home situations where infant growth is faltering. One UK study (Onozawa et al 2001) reported more effective interactions which were warmer and less intrusive, between post-natally depressed mothers and their infants following a five week infant massage course. This is an important finding but raises questions about individual teaching methods and how much attention was drawn to responding to infants’ cues. While massage may be an effective medium for encouraging parental sensitivity and awareness of infant communication, however this may be dependent on the training and aptitude of the instructor. Conclusions Potentially valuable benefits on aspects of maternal behaviour and infant behaviour, development and physiology were evident in a small number of studies. No evidence of harm was identified. Robust trials are needed to confirm these findings and to assess whether the geographical differences we observed are attributable to study methodology, approaches to massage or to cultural differences. Meanwhile, the equivocal findings of this review provide insufficient evidence on which to base decisions regarding either the development of new provision or the discontinuation of existing provision of services to teach massage to parents of low risk infants in community settings. 17 It would be beneficial to have more research into specific methods of teaching infant massage and the possible role it can play as a medium for promoting infant –parent communication. Among the non-institutionalised low-risk infants who were the subject of this review, massage was associated with benefits in growth only in studies at high risk of bias. Further robust trials are clearly needed in different parts of the world to confirm the positive findings of this review with regard to sleep, crying and physiological effects which were based on a limited number of studies. These trials should also measure growth to establish whether the discrepant results we observed are attributable to methodological inadequacies or cultural differences in either approaches to massage or normal infant care. Such research should aim to distinguish effects in infants in homes where care is optimal from those where it is less than optimal. There is also a need for further research on the effect of infant massage on parent-infant interaction and infant temperament where findings of this review were inconclusive. Bibliography Ainsworth, M. (1973) The development of infant-mother attachment. In: B. Caldwell and H, Ricciuti (Eds) Review of child development research. Vol 3, 1-94. Argawal K, Ashish G, Pushkarna R, Bhargava S, Prabhu M. Effects of massage and use of oil on growth, blood flow and sleep patterns in infants. Indian Journal of Medical Research 2000; 112:212-217. Blackwell, P. (2000) The Influence of Touch on Child Development: Implications for Intervention. Infants and Young Children, 25-39. Brazelton, T. B. (1990) The earliest relationship. Reading, MA: Addison Wesley. Brunner E. Socioeconomic determinants of health: Stress and the biology of inequality. British Medical Journal 1997; 314:1472. Carver, R. and Carver, L. (2003) The basal ganglia: a neural network with more than motor function. Seminars Pediatric Neurology Mar;10(1):3-10. Chugani, H. (1996) Neuroimaging of developmental nonlinearity and developmental pathologies. In R. Thatcher, G. Reid Lyon, J. Rumsey, and N. Krasnegor (Eds) Developmental neuro-imagining: Mapping the development of the brain and behavior 187-195. San Diego: Academic Press. 18 Cigales M, Field T, Lundy B, Cuadra A, Hart S. Massage enhances recovery from habituation in normal infants. Infant Behavior and Development 1997; 20(1):29-34. Cohen S, Kaplan JR, Cunnick JE, Manuck SB, Rabin BS. Chronic social stress, affiliation, and cellular immune response in nonhuman primates. Psych Sci 1992; 3:301-304. Cited in: Brunner E. (1997) Socioeconomic determinants of health: Stress and the biology of inequality. British Medical Journal 314, 1472. Darmstadt G, Samir K Saha. Traditional practice of oil massage of neonates in Bangladesh Journal of Health, Population and Nutrition 2002; 20(2):84-8. De Chateau, P. (1976) The influence of early contact on maternal and infant behavior on primaparae. Birth and Family Journal 3, 149-155. Duan Lihong, Li Weihong, Shi Fentao. Studying impact of touching on growth and development of infants. Chinese Nursing Research 2002; 16:5. Elliot MR, Reilly SM, Drummond J, Letourneau N. The effect of different soothing interventions on infant crying on parent-infant interaction. Infant Mental Health Journal 2002; 23(3):310-328. Field, T. (2000). Infant Massage Therapy. In: C. H.J. Zeanah (Ed) Handbook of Infant Mental Health. New York, Guilford Press. 2nd Edition. 494-500. Field T, Grizzle N, Scafidi F, Abrams S, Richardson S. Massage therapy for infants of depressed mothers. Infant Behaviour and Development 1996; 19:107-112. Field T, Pickens J, Prodromidis M, Malphurs J, Fox N. Targeting adolescent mothers with depressive symptoms for early intervention Adolescence 2000;35(138):381-414. Field T, Schanberg S, Davalos M, Malphurs J. Massage with oil has more positive effects on normal infants. Journal of Prenatal and Perinatal Psychology and Health 1996;11(2):75-80. Goldstein Ferber SG, Laudon M, Kuint J, Weller A, Zisapel N. Massage therapy by mothers enhances the adjustment of circadian rhythms to the nocturnal period in full-term infants. Developmental and Behavioral Pediatrics 2002; 23(6):410-415. Goosen, C. (1981) Abnormal behavior patterns in rhesus monkeys: symptoms of mental disease? Biological Psychiatry 16: 697-716. Greenhough, W. and Black, J. (1992) Induction of brain structure by experience. Substates for cognitive development. In M. Gunnar and C.Nelson (Eds) Minnesota Symposium on Child Psychology. Vol 24 Developmental Behavioral Neuroscience 155-200. Hillsdale NJ: Erlbaum. Gunnar, M. (1998) Quality of early care and buffering of neuroendocrine stress reactions: Potential effects on the developing human brain. Preventive Medicine 27, 208-211. Gunnar M, Broderson L, Rigatuso J. 'Infant and Parent Contributions to the organization of adrenocorticol stress reactivity' Paper presented at the symposium on the development and organization of stress reactivity at the biennial meeting of the Society for Research in Child Development in 19 New Orleans, 1998. (Cited in: Zeanah, C. (2000) Handbook of Infant Mental Health. New York: Guilford. Gunnar, M. and Donzella, B. (2002) Social Regulation of the cortisol levels in early human development. Psychoneuroendocrinology 27, 199-220. Gunnar, M. and Vazquez, D. (2001) Low cortisol and a flattening of expected daytime rhythm: Potential indices of risk in human development. Development and Psychopathology 13: 515-538. Harlow, H. (1958) The nature of love. American Psychologist, 13, 673-685. Harlow, H. (1965) Total isolation: Effects on macaque monkey behaviour, Science, 148, 666. Harlow, H. and Harlow, M. (1971) Psychopathology in monkeys. In: H. Kimmel (Ed) Experimental Psychopathology. New York: Academic Press. Johnson, D. 2000. The impact of orphanage rearing on growth and development. In: Nelson, C.A., (Ed) 2000. The Effects of Adversity on Neurobehavioral Development: Minnesota Symposia on Child Psychology 31, Lawrence Erlbaum, Mahwah, NJ, pp. 113–162. Johnson, E. Kamilaris, T., Chrousos, G. and Gold, P. (1992). Mechanisms of stress: a dynamic overview of hormonal and behavioral homeostasis. Neuroscience Biobehavioral Reviews. 16, pp. 115–130. Jump V. Effects of infant massage on aspects of the parent-child relationship: an experimental manipulation. Unpublished thesis: Utah State University, 1998. Ke G, Ling X, Li L. Clinical survey of improved massage method developing infants' growth and development. China Nurse 2001; 36(4);278-280. Kim T I, Shin YH, White-Traut AC. Multisensory intervention improves physical growth and illness rates in Korean orphaned newborn infants. Research in Nursing & Health 2003; 26(6):424-33. Koniak Griffin D, Ludington-Hoe S, Verzemnicks I. Longitudinal effects of unimodal and multimodal stimulation on development and interaction of healthy infants. Research in Nursing and Health 1995; 18: 27-38. Koniak Griffin D, Ludington-Hoe S, Verzemnicks I. Longitudinal effects of unimodal and multimodal stimulation on development and interaction of healthy infants. Research in Nursing and Health 1995; 18:27-38. Koniak-Griffin D, Ludington-Hoe S, Verzemnieks I. Developmental and temperament outcomes of sensory stimulation in healthy infants. Nursing Research 1988; 37(2):70-76. Kraemer, G. (1985) The psychobiology of attachment and separation (Reite, M. and Field, T. (Eds) 135-161 New York: Academic. Liu, D. Diorio, J. Tannenbaum, B. Caldji, C. Francis, D. Freedman, A. Sharma, S. Pearson, D. Plotsky, P. and Meaney, M. (1997) Maternal Care, hippocampal glucocortoid receptors, and hypothalamic-pituitary responses to stress. Science, 277, 1659-1662. Liu Chun Li. The effect of touching on healthy infants' weight. Journal of Huaihai Medicine. 2005; 23(2):137. 20 Liu D, Diorio J, Tannenbaum B. Maternal Care, hippocampal glucocorticoid receptors and hypothalamic-pituitary-adrenal responses to stress. Science 1997; 277:1659-1662. Liu DY. Clinical experience in infant massage. 100 case studies. Chongqing Medicine 2005; 34(7):301. Lu Jiao, Li Ju Zhan, Wu Li Fang. A study of the effect of touch on health in infants. Practical Clinical Medicine 2005; 6(2):119-121. Martin, L. Spicer, D. Lewis, M. Gluck, J. and Cork, L. (1991) Social Deprivation of Infant Rhesus Monkeys Alters Chemoarchitecture of the Brain: I. Subcortical Regions. The Journal of Neuroscience, 11 (11) 3344-3358. Mitchell, G. (1970) Primate Behaviour. Developments in field and laboratory research (Rosenblum LA ed) 195-217 New York: Academic. Moszkowski, R. and Stack, D. (2007) Infant Touching Behaviour During MotherInfant Face-to-Face Interactions. Infant and Child Development 16, 307319. Na Zhuo Hua, Xie Hui Yun, Huang Jian Hua. The effect of infant massage on growth. New Journal of Traditional Chinese Medicine 2005; 37(5):69-70. Nelson, C. and Bosquet, M. (2000) Neurobiology of Fetal and Infant Development: Implications for Infant Mental Health. Ch 3. Cited in Zeanah, C.H. Jr. (Ed) (2000) Handbook of Infant Mental Health. Second Edition. New York: Guilford Press. Onozawa K, Glover V, Adams D, Modi N, Kumar R C. Infant massage improves mother-infant interaction for mothers with postnatal depression. Journal of Affective Disorders 2001; 63:201- 207. Rogoff, B. (2003) The Cultural Nature of Human Development. Oxford: Oxford University Press. Scafidi F, Field T. Massage therapy improves behavior in neonates born to HIVpositive mothers. Journal of Pediatric Psychology 1996;21(6):889-97 Schanberg S. Genetic basis for touch effects. In Field, T. Touch in early development. Hillsdale, New Jersey: Erlbaum, 1994. Schanberg S. Genetic basis for touch effects. In Field, T. Touch in early development. Hillsdale, New Jersey: Erlbaum, 1994. Schore, A. (2003) Affect dysregulation and disorders of the self. New York: Norton. Shao L et al. The effect of infant massage on health: a nursing experience. Journal of Chinese Clinical Research 2005; 11(11):1582-1583. Shi Li, Xue Li Rong. The clinical observation of touching towards the neonatal health's affection. Journal of Henan University 2002; 21(4):26-27. Sun Hai Yun, Gao Xiang Yu, Zhao Xue Mei. A comparative study on influence of touching on growth, development and jaundice of normal infants. Chinese Nursing Research 2004; 18(8b):1468-1469. Underdown A, Barlow J, Chung V, Stewart-Brown S. Massage intervention for promoting mental and physical health in infants aged under six months. The Cochrane Library, Issue 6, 2006. 21 Uvnas-Moberg K, Widstrom AM, Marchini G, Windberg J. Release of GI hormones in mother and infant by sensory stimulation. Acta Paediatrica Scandinavica 1987; 76:851-60. Vickers A, Niraj G, Harland R, Rees R. Do certain countries produce only positive results? A systematic review of controlled trials. Controlled Clinical Trials 1997; 19:159-166. Vickers A, Ohlsson A, Lacy JB, Horlsey A. Massage for promoting growth and development of preterm and/or low birthweight infants. Cochrane Library, Issue 4, 2004. Wang Bin, Shen Yue Hua, Jin Run Yan et al. Improving infant growth by massage: a clinical study. Chinese Journal of Perinatal Medicine 1999; 2(4):241-242. Xua Li Shuan, Qing Gui Romg, Ye Mei Yan et al. Study of touch intervention of infant sleep disorder. Journal of Nursing Continual Education 2004; 19(11):973-976. Ye Hong Yun. Clinical observation on infant massage. Journal of Gan Nan Medical College 2004; 3:239-240. Zhai J, Pan Xian R, Hua JR et al. The effect of massage on growth: a clinical study. Journal of Sichuan continuing Education College of Public;Health and Managerial Sciences 2001;20(10):23. 22