Meta-analysis of physiological effects of skin-to-skin contact for newborns and mothers

Original Articleped_2909 161..170

Meta-analysis of physiological effects of skin-to-skin contact fornewborns and mothers

Rintaro Mori,1–3 Rajesh Khanna,2 Debbie Pledge2 and Takeo Nakayama3

1Osaka Medical Center and Research Institute for Maternal and Child Health, Izumi, 3Kyoto University, School of PublicHealth, Kyoto, Japan and 2National Collaborating Centre for Women’s and Children’s Health, London, UK

Abstract Background: Skin-to-skin care has been adopted all over the world, although physiological changes during or after ithave not been evaluated very well. The purpose of the present study was therefore to investigate whether skin-to-skincontact for newborn babies and their mothers affects body temperature, heart rate and oxygen saturation of the babies.Methods: Studies investigating body temperature, heart rate and oxygen saturation of babies during and/or afterskin-to-skin contact were systematically searched and reviewed. Meta-analyses to examine the effects and meta-regression analyses to investigate correlations between the effects and birthweight, duration of the care, environmentaltemperature, and resources of the setting, were conducted.Results: A total of 23 studies were included. Meta-analyses showed evidence of an increase in body temperature(weighted mean difference [WMD] 0.22°C, P < 0.001) and a decrease in saturation of babies (WMD -0.60%; P = 0.01)during skin-to-skin care, compared with those before skin-to-skin care. Increase in body temperature was more evidentin middle–low-income settings (WMD, 0.61°C, P < 0.001) than high-income settings (WMD 0.20°C, P < 0.001). Boththe positive effect on body temperature and the negative effect on saturation were more marked in cold environmentsthan where the environmental temperature was higher (WMD 0.18°C, P < 0.001; WMD -0.82%, P = 0.02).Conclusion: Skin-to-skin care is effective in increasing the body temperature of babies, especially where resources arelimited and the environment is cold. Decreased oxygen saturation of the babies, however, warrants further prospectivestudies to confirm the findings.

Key words meta-analysis, infant, patient safety, skin-to-skin, systematic review.

Kangaroo Mother Care is originally a package of care includingcontinuous skin-to-skin contact and exclusive breast-feeding forlow-birthweight infants and their mothers.1 The package wasinvented in Colombia as an alternative to an incubator, and hasspread around the world, mainly where resources are relativelylimited.2 A systematic review as well as randomized controlledtrials on this care found significantly better cost and clinicaleffectiveness including reduction in neonatal morbidity, increasein breast-feeding rates, and improved psychological and behav-ioral change in both mothers and babies, compared with standardincubator care in such settings.1

This care has also been adopted in relatively affluent areas tofacilitate mother–infant bonding as well as to promote breast-feeding. The adaptations include (i) skin-to-skin care immedi-ately after birth for term infants and their mothers,3 and (ii)intermittent skin-to-skin care for stable low-birthweight infants.4

Previous studies have found greater benefit for these adapta-tions of skin-to-skin care of newborn infants and their mothers inrelatively affluent settings, compared with standard care. Theseinclude increase in breast-feeding rates, and positive psychologi-cal and behavioral impact on both mothers and babies.1 Inclusioncriteria for this care, however, particularly in areas of relativeaffluence have not been well established. There have been reportsof further exploration of skin-to-skin care for sick low-birthweight infants even on mechanical ventilators,5–9 and con-tinuous skin-to-skin care for all low-birthweight infants inmodern neonatal intensive care.10

Previous studies have attempted to address the potentialadverse effects of skin-to-skin care, particularly hypothermia,apnea of prematurity and respiratory state.11 The vast majority ofsuch studies conducted in relatively resource-affluent settingswere before–after studies with a relatively small sample size;hence the question remains unanswered.12 Recently there havebeen several reports of ‘apparently life-threatening events’ inboth term and preterm newborns who were having skin-to-skincare.13,14 Therefore there is need for greater understanding of thephysiological status of babies during skin-to-skin care.

The aim of the present study was therefore to investig-ate whether skin-to-skin contact for both low- and

Correspondence: Rintaro Mori, MD, PhD, MSc, FRCPCH, Division ofStrategic Planning and Collaboration, Osaka Medical Center andResearch Institute for Maternal and Child Health, 840 Murodocho,Izumi, Osaka 594-1101, Japan. Email: [email protected]

Received 21 May 2008; revised 18 May 2009; accepted 2 June 2009.

Pediatrics International (2010) 52, 161–170 doi: 10.1111/j.1442-200X.2009.02909.x

© 2010 Japan Pediatric Society

mailto:[email protected]

normal-birthweight infants and their mothers alters physiologicalparameters including temperature, heart rate and saturation.

Methods

The criteria for inclusion into the present systematic review wereas follows.

Types of studies

Comparison of physiological parameters of infants before start-ing skin-to-skin contact with parameters during and/or afterskin-to-skin contact was the main criterion. The most likelystudy designs were before-and-after studies, although data fromrandomized controlled trials and cohort studies were alsoconsidered.

Types of participants

Newborn infants aged up to 28 days old were considered. Sub-group analysis of low- and normal-birthweight infants wasplanned. Infants with chronic lung disease, congenital heartdisease, and those on mechanical ventilators were excluded,because their usual physiological values were considered signifi-cantly different from infants without these conditions. Gesta-tional age and birthweight were included in a meta-regressionanalysis.

Types of intervention

Skin-to-skin contact between mother and newborn infantsregardless of duration was considered. Duration of contact wasincluded in a meta-regression analysis.

Types of outcomes measures

For all three parameters, mean differences and their standarddeviations before and during, as well as for before and after, wereextracted from included studies. Details of measurement of bodytemperature, heart rate and saturation are as follows.

Body temperature of infants

Temperature was measured either axially or rectally, before,during and after skin-to-skin contact. When studies used bothaxial and rectal measurements, rectal measurement was used: thiswas regarded to reflect the core temperature of infants, and ishence clinically more important.

Heart rate of infants

Heart rate was measured using monitoring devices, before,during and after skin-to-skin contact. Heart rate measurementwas taken as an average of certain observation periods. Details ofmeasurement in each of the included studies are described inTable 1.

Oxygen saturation of infants

Saturation was measured through the skin using monitoringdevices, before, during and after skin-to-skin contact. Saturationmeasurement was taken as an average of certain observationperiods. Details of measurement in each of the included studiesare described in Table 1.

Search strategy for identification of studies

An information specialist conducted a systematic search of thefollowing online databases: MEDLINE (1966–August 2006);EMBASE (1980–August 2006); CINAHL (1982–August 2006);Cochrane Central Register of Controlled Trials (3rd quarter2006); POPLINE; LILACS; and African Index Medicus.

The main subject headings and free text terms used were:‘kangaroo’; ‘kmc’; ‘skin to skin’; ‘infant’; ‘baby’; ‘newborn’;‘neonate’. The search was not limited by language; the searchwas limited to humans. No attempt was made to search grayliterature (i.e. literature that is not published in academic peerreviewed journals and available through indexed databases forreview).

Review procedure

Two reviewers (RM and RK) independently assessed the meth-odological quality of each identified study, and any discrepancyin quality assignment was planned to be solved in discussion withthe third reviewer (TN), although no discrepancies occurred.

Weighted mean difference (WMD) and confidence intervalswere calculated for each comparison. A meta-regression analysiswas conducted to investigate correlations between the effects andother potential effect modifiers including low/normal birth-weight, duration of skin-to-skin contact, annual average tempera-ture of the city where the study was conducted (as a proxy for theenvironmental temperature), and resource of the setting (high ormiddle–low income). When evidence of correlation was found inthe meta-regression analysis, subgroup analysis by the param-eter(s) was conducted. Birthweight and duration of skin-to-skincare were extracted as either means or medians from the includedstudies. The income status (high, middle or low), defined by theWorld Bank,15 was also extracted from included studies. Annualaverage temperature of the city where each study was conductedwas obtained from the Global Historical Climatology Network.16

Duration of skin-to-skin care and temperature of the city wasexamined as a continuous variable in the meta-regression analy-sis, but when they were found to be related to the effects, 10°Cfor the city temperature and 90 min for the duration of skin-to-skin contact were used as the cut-offs for the subgroup analyses.These cut-offs were used for the sake of convenience only.

Ethics approval

This study was conducted using original articles that have beenpublished in the public domain, therefore the obtaining of ethicsapproval was considered unnecessary.

Results

Description of studies

The search yielded 1087 citations. A total of 47 potentially rel-evant articles were obtained for further assessment. Of these 47articles, 24 articles (23 studies) were included in the review(Table 1);11,17–39 the remaining 23 articles were excluded.7,40–61

The reasons for exclusion included (i) not giving SD in eightarticles;40,45,52,54,55,57,59,60 (ii) point estimates were provided bymedian and/or range in five articles;42–44,49,56 (iii) data shown only

162 R Mori et al.


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Meta-analysis of skin-to-skin contact 163


in a graphical manner in two articles;41,53 (iv) only single mea-surement provided in two articles;47,51 (v) only proportion ofbabies with hypothermia presented in one article;46 (vi) only heartrate variability presented in one article;48 (vii) heart rate measuredbut not presented in one article;50 (viii) outcome reported asstability of cardiorespiratory system in preterm infants (SCRIP)score in one article;58 (ix) case report format of one baby andskin-to-skin care provided with mechanical ventilation;7 and (x)case report format of five babies with congenital heart diseasesrequiring open heart surgery.61

Among the included 23 studies, 13 studies used case-series(before–after studies),19–25,28–30,34,35,38 five studies were randomizedcontrolled trials and only data from the arm in which babies hadskin-to-skin care were extracted,11,17,18,32,33 one study was a cross-over trial,27 and the remaining four were cohort studies.26,31,36,37,56

Eighteen studies were conducted in high-income countries(nine in the USA,11,17,18,21,22,24,30,34,36,38 three in Germany,19,23,25 threein Spain,31,33,35 one in Canada,26 one in the UK28 and one inSweden29), while one was in an upper–middle-income country(Russia),32 three were in lower–middle-income countries (two inColombia20,37 and one in Taiwan39) and one in a low-incomecountry (Nigeria).27

Fifteen studies measured body temperature, heart rate and/orsaturation of low-birthweight infants,11,17–28,34,35,37 and the remain-ing eight studies measured these in term and normal-birthweightinfants.29–33,36,38,39

The UK study reported results for both preterm infants withnormal lungs and with chronic lung disease.28 Only the data forthose with normal lungs were extracted for the present review.

Methodology

The included studies were reasonably homogenous. Heterogene-ity in reporting and measuring the physiological parameters wasfound. Studies used different criteria for stable babies, and somestudies did not provide detailed criteria.

Findings

Body temperature

Compared with the body temperature prior to skin-to-skin care,there was strong evidence of an increase in body temperatureduring skin-to-skin care by 0.22°C (22 studies, WMD 0.22°C;95% confidence interval [CI]: 0.18–0.27, P < 0.001), and afterskin-to-skin care by 0.14°C (12 studies, WMD 0.14; 95%CI:0.09–0.18, P < 0.001; Figs 1,2).

When meta-regression was conducted, there was strong evi-dence that the effect on body temperature during skin-to-skincare compared with that before skin-to-skin care was correlatedwith income status of the country (P = 0.007) and borderlineevidence that it was correlated with the temperature of the city(P = 0.06). No evidence was found for correlation with birth-weight and duration of skin-to-skin care (Table 2). Therefore, theresults of meta-analysis of the effect on body temperature during

Review: Physiological changes of newborn babies during skin-to-skin care

Comparison: 01 Physiological changes (During SSC - Pre SSC)

Outcome: 01 Body temperature

)dexif( DMW thgieW )dexif( DMW Before gniruD ydutS

raeY IC %59 % IC %59 )DS( naeMn)DS( naeMnyrogetac-bus ro

01 High income countries

Bauer 1997 22 35.60(1.00) 22 35.00(0.70) 0.69 0.60 [0.09, 1.11] 1997

Bosque 1995 8 36.50(0.64) 8 36.80(0.27) 0.77 -0.30 [-0.78, 0.18] 1995

Chiu 2005 39 36.80(0.20) 39 36.70(0.30) 13.98 0.10 [-0.01, 0.21] 2005

Christensson 1992 25 37.10(0.37) 25 36.60(0.47) 3.26 0.50 [0.27, 0.73] 1992

Christensson 1995 14 36.90(0.40) 14 36.00(0.50) 1.59 0.90 [0.56, 1.24] 1995

Clifford 2001 7 36.76(0.34) 7 36.76(0.33) 1.45 0.00 [-0.35, 0.35] 2001

Durand 1997 25 37.20(0.29) 25 36.90(0.40) 4.77 0.30 [0.11, 0.49] 1997

Fohe 2000 53 37.30(0.30) 53 37.00(0.30) 13.72 0.30 [0.19, 0.41] 2000

Gardner 1979 10 36.72(0.16) 10 37.33(0.11) 12.36 -0.61 [-0.73, -0.49] 1979

Karlsson 1996 9 34.70(0.40) 9 34.10(0.40) 1.31 0.60 [0.23, 0.97] 1996

Legault 1995 61 37.30(0.30) 61 36.60(0.30) 15.79 0.70 [0.59, 0.81] 1995

Ludington 1991 12 36.89(0.44) 12 36.05(0.61) 0.99 0.84 [0.41, 1.27] 1991

Ludington 2000 16 36.90(0.31) 16 36.69(0.38) 3.10 0.21 [-0.03, 0.45] 2000

Ludington 2004 11 36.99(0.36) 11 36.33(0.95) 0.50 0.66 [0.06, 1.26] 2004

Monasterolo 1998 38 36.80(0.30) 38 36.80(0.30) 9.84 0.00 [-0.13, 0.13] 1998

Wieland 1995 39 37.25(0.33) 39 37.02(0.28) 9.70 0.23 [0.09, 0.37] 1995

Subtotal (95% CI) 389 389 93.83 0.20 [0.15, 0.24]

Test for heterogeneity: Chi² = 320.57, df = 15 (P < 0.00001), I² = 95.3%

Test for overall effect: Z = 8.86 (P < 0.00001)

02 Middle-low income countries

Bystrova 2003 44 36.20(1.51) 44 34.50(1.21) 0.55 1.70 [1.13, 2.27] 2003

Huang 2002 24 37.30(0.40) 24 37.00(0.40) 3.50 0.30 [0.07, 0.53] 2002

Ibe 2004 13 37.60(0.50) 13 37.10(0.80) 0.68 0.50 [-0.01, 1.01] 2004

Ludignton 1999 6 37.30(0.40) 6 36.30(0.78) 0.36 1.00 [0.30, 1.70] 1999

Ludington 1992 11 37.45(0.30) 11 36.43(0.62) 1.08 1.02 [0.61, 1.43] 1992

Subtotal (95% CI) 98 98 6.17 0.61 [0.44, 0.78]



Total (95% CI) 487 487 100.00 0.22 [0.18, 0.27]



-4 -2 0 2 4

Decrease Increase

Fig. 1 Forest plot: effect on body temperature during skin-to-skin care, compared with that before skin-to-skin care, stratified by resource ofsettings. CI, confidence interval; SSC, skin-to-skin care; WMD, weighted mean difference.

164 R Mori et al.


skin-to-skin care were stratified by the income status of thecountries (Fig. 1). Subgroup analysis showed strong evidence ofa higher increase in body temperature in middle–low-incomecountries (five studies, WMD 0.61°C; 95%CI: 0.44–0.78) com-pared to high-income countries (16 studies, WMD 0.20°C;95%CI: 0.15–0.24). When the body temperature of the babiesafter skin-to-skin care was compared with that before skin-to-skin care, however, there was a strong evidence of a correlationbetween the effect and the temperature of the city (P = 0.004).There was no evidence of correlation with the other parameters.The results of meta-analysis of the effect on body temperatureafter skin-to-skin care was stratified by temperature of the cityand divided into two categories: studies conducted in cities wherethe annual average temperature is 210°C, and those in citieswhere the temperature is higher (Fig. 2). The subgroup analysisshowed strong evidence of an increase in body temperature afterskin-to-skin care in cities where the average temperature was210°C (five studies, WMD 0.18°C; 95%CI: 0.13–0.23), but theeffect was not sustained after skin-to-skin care in cities where theaverage temperature was >10°C (seven studies, WMD 0.00°C;95%CI: -0.10 to 0.10).

Heart rate

Overall there was no evidence of a difference in heart ratebetween before and during skin-to-skin care (12 studies, WMD2.04 beats/min; 95%CI: -0.04 to 4.12), and no evidence betweenbefore and after skin-to-skin care (10 studies, WMD -0.07 beats/min; 95%CI: -2.27 to 2.13; Figs 3,4). When a meta-regressionanalysis was conducted, however, to examine the relationshipbetween the effect on heart rate during skin-to-skin care and otherparameters, there was evidence of a correlation between the

effect and income of the country (P = 0.04) only (Table 2). Onstratifying the effect on heart rate by income status of the coun-tries, there was evidence of an increase in heart rate by 2.82beats/min during skin-to-skin care in high-income countries, butno evidence of such effect in middle–low-income countries(Fig. 3).

Oxygen saturation

Overall, there was evidence that saturation of babies during skin-to-skin care was decreased by 0.60% (10 studies, WMD -0.60%;95%CI: -1.05 to -0.15), but only borderline evidence that suchan effect remained after skin-to-skin care (eight studies, WMD-0.48%; 95%CI: -0.97 to 0.02; Figs 5,6).

When meta-regression was conducted, there was no evidenceof a correlation between the effect on saturation during skin-to-skin care and the parameters; therefore no subgroup analysis wasconducted. There was borderline evidence, however, of a corre-lation between the effect after skin-to-skin care and the tempera-ture of the cities (P = 0.05). The effect on saturation after skin-to-skin care was stratified by the temperature of the cities.Subgroup analysis showed that there was evidence that adecrease in saturation remained after skin-to-skin care in citieswhere the annual average temperature was 210°C (three studies,WMD -0.82%; 95%CI: -1.48 to -0.15), but there was no sucheffect observed in the warmer cities (five studies, WMD -0.03;95%CI: -0.79 to 0.72; Fig. 6).

Funnel plots of all the results of the meta-analyses wereexamined to assess possibility of publication bias. No evidenceof publication bias was observed. Duration of skin-to-skin caredid not alter the association in any of the three physiologicalparameters.


Comparison: 02 Physiological changes (Post SSC - Pre SSC)

Outcome: 01 Body temperature


IC %59 % IC %59 )DS( naeMn)DS( naeMnyrogetac-bus ro

01 Temperature of the city 10 Celsius degree or lower

Legault 1995 61 36.90(0.30) 61 36.60(0.30) 19.89 0.30 [0.19, 0.41]

Fohe 2000 53 37.20(0.20) 53 37.00(0.30) 23.93 0.20 [0.10, 0.30]

Bauer 1997 22 35.10(0.70) 22 35.00(0.70) 1.32 0.10 [-0.31, 0.51]

Wieland 1995 39 37.10(0.30) 39 37.02(0.28) 13.59 0.08 [-0.05, 0.21]

Chiu 2005 39 36.80(0.20) 39 36.70(0.30) 17.61 0.10 [-0.01, 0.21]

Subtotal (95% CI) 214 214 76.33 0.18 [0.13, 0.23]

Test for heterogeneity: Chi² = 9.42, df = 4 (P = 0.05), I² = 57.5%


02 Temperature of the city higher than 10 Celsius degree

Ludington 2000 16 36.65(0.34) 16 36.69(0.38) 3.61 -0.04 [-0.29, 0.21]

Ludington 2004 11 36.40(0.87) 11 36.33(0.95) 0.39 0.07 [-0.69, 0.83]

Clifford 2001 7 36.74(0.28) 7 36.76(0.33) 2.19 -0.02 [-0.34, 0.30]

Bosque 1995 8 36.70(0.26) 8 36.80(0.27) 3.34 -0.10 [-0.36, 0.16]

Monasterolo 1998 38 36.80(0.30) 38 36.80(0.30) 12.39 0.00 [-0.13, 0.13]

Ludington 1991 12 36.46(0.49) 12 36.05(0.61) 1.15 0.41 [-0.03, 0.85]

Ibe 2004 13 37.10(0.80) 13 37.10(0.80) 0.60 0.00 [-0.62, 0.62]

Subtotal (95% CI) 105 105 23.67 0.00 [-0.10, 0.10]

Test for heterogeneity: Chi² = 4.01, df = 6 (P = 0.68), I² = 0%

Test for overall effect: Z = 0.02 (P = 0.98)

Total (95% CI) 319 319 100.00 0.14 [0.09, 0.18]



-1 -0.5 0 0.5 1

Decrease Increase

Fig. 2 Forest plot: effect on body temperature during skin-to-skin care, compared with that before skin-to-skin care, stratified by temperatureof the cities. CI, confidence interval; SSC, skin-to-skin care; WMD, weighted mean difference.



Tabl

e2

Res

ults

ofm

eta-

anal

ysis

and

met

a-re

gres

sion

Met

a-an

alys

isE

ffec

tsdu

ring

skin

-to-

skin

care

,com

pare

dw

ithbe

fore

skin

-to-

skin

care

Bod

yte

mpe

ratu

re(°

C)

Hea

rtra

te(b

eats

/min

)Sa

tura

tion

(%)

No.

stud

ies

2112

10O

vera

llre

sults

0.22

[0.1

8–0.

27)

P<

0.00

12.

04(-

0.04

to4.

12)

P=

0.05

-0.6

0(-

1.05

to-0

.15)

P=

0.01

Test

for

hete

roge

neity

I2=

94.6

%P

<0.

001

I2=

27.8

%P

=0.

17I2

=12

.7%

P=

0.33

Met

a-re

gres

sion

anal

ysis

Cor

rela

tion

coef

ficie

ntP

Cor

rela

tion

coef

ficie

ntP

Cor

rela

tion

coef

ficie

ntP

No.

stud

ies

2112

10Te

mpe

ratu

reof

the

city

°C-0

.05

0.06

0.64

0.17

0.07

0.51

Inco

me

ofth

eco

untr

yhi

gh/m

id-l

ow0.

820.

007

-14.

470.

04-0

.59

0.70

Bir

thw

eigh

tlo

w/n

orm

al0.

040.

85N

/AN

/AD

urat

ion

ofsk

in-t

o-sk

inca

redu

ratio

n(m

in)

0.00

20.

250.

140.

55-0

.001

0.88

Met

a-an

alys

isE

ffec

tsaf

ter

skin

-to-

skin

care

,com

pare

dw

ithbe

fore

skin

-to-

skin

care

Bod

yte

mpe

ratu

re(°

C)

Hea

rtra

te(b

eats

/min

)Sa

tura

tion

(%)

No.

stud

ies

1210

8O

vera

llre

sults

0.14

(0.0

9–0.

18)

P<

0.00

1-0

.07

(-2.

27to

2.13

)P

=0.

95-0

.48

(-0.

97to

0.02

)P

=0.

06Te

stfo

rhe

tero

gene

ityI2

=53

.2%

P=

0.01

I2=

0%P

=0.

86I2

=0%

P=

0.81

Met

a-re

gres

sion

anal

ysis

Cor

rela

tion

coef

ficie

ntP

Cor

rela

tion

coef

ficie

ntP

Cor

rela

tion

coef

ficie

ntP

No.

stud

ies

1210

8Te

mpe

ratu

reof

the

city

Cel

sius

degr

ee-0

.03

0.00

40.

370.

200.

110.

05In

com

eof

the

coun

try

high

/mid

-low

0.34

0.25

N/A

N/A

Bir

thw

eigh

tlo

w/n

orm

al-0

.64

0.38

N/A

N/A

Dur

atio

nof

skin

-to-

skin

care

dura

tion(

min

)-0

.000

40.

610.

008

0.56

-0.0

010.

82

166 R Mori et al.




Outcome: 02 Heart rate



01 High income countries

Acolet 1989 9 158.70(9.20) 9 152.20(8.50) 6.44 6.50 [-1.68, 14.68] 1989

Bauer 1997 22 151.00(10.00) 22 151.00(9.00) 13.65 0.00 [-5.62, 5.62] 1997

Bosque 1995 8 161.00(12.40) 8 160.00(11.20) 3.22 1.00 [-10.58, 12.58] 1995

Clifford 2001 7 163.63(11.25) 7 162.78(11.10) 3.15 0.85 [-10.86, 12.56] 2001

Fohe 2000 53 149.00(16.00) 53 144.00(14.00) 13.16 5.00 [-0.72, 10.72] 2000

Legault 1995 61 148.50(19.60) 61 151.10(16.70) 10.33 -2.60 [-9.06, 3.86] 1995

Ludington 1991 12 154.77(15.23) 12 145.38(6.83) 4.84 9.39 [-0.05, 18.83] 1991

Ludington 2004 11 152.17(10.84) 11 144.04(9.61) 5.88 8.13 [-0.43, 16.69] 2004

Messmer 1997 20 160.54(11.60) 20 160.34(11.00) 8.79 0.20 [-6.81, 7.21] 1997

Monasterolo 1998 38 152.40(16.10) 38 150.10(18.80) 6.96 2.30 [-5.57, 10.17] 1998

Wieland 1995 39 158.00(12.00) 39 154.00(12.00) 15.20 4.00 [-1.33, 9.33] 1995

Subtotal (95% CI) 280 280 91.61 2.82 [0.65, 4.99]



02 Middle-low income countries

Huang 2002 24 135.10(13.40) 24 141.60(11.90) 8.39 -6.50 [-13.67, 0.67] 2002

Subtotal (95% CI) 24 24 8.39 -6.50 [-13.67, 0.67]

Test for heterogeneity: not applicable


Total (95% CI) 304 304 100.00 2.04 [-0.04, 4.12]



-10 -5 0 5 10

Decrease Increase

Fig. 3 Forest plot: effect on heart rate during skin-to-skin care, compared with that before skin-to-skin care, stratified by resource of thesettings. CI, confidence interval; SSC, skin-to-skin care; WMD, weighted mean difference.



Outcome: 02 Heart rate

)dexif( DMW thgieW )dexif( DMW Before After ydutS


Bauer 1997 22 151.00(11.00) 22 151.00(9.00) 13.70 0.00 [-5.94, 5.94] 1997

Bosque 1995 8 160.00(9.70) 8 160.00(11.20) 4.58 0.00 [-10.27, 10.27] 1995

Clifford 2001 7 164.46(12.31) 7 162.78(11.10) 3.21 1.68 [-10.60, 13.96] 2001

Fohe 2000 53 145.00(16.00) 53 144.00(14.00) 14.75 1.00 [-4.72, 6.72] 2000

Legault 1995 61 147.40(13.60) 61 151.10(16.70) 16.54 -3.70 [-9.10, 1.70] 1995

Ludington 1991 12 148.88(11.22) 12 145.38(6.83) 8.75 3.50 [-3.93, 10.93] 1991

Ludington 2004 11 148.19(11.97) 11 144.04(9.61) 5.87 4.15 [-4.92, 13.22] 2004

Messmer 1997 20 156.99(11.00) 20 160.34(11.00) 10.40 -3.35 [-10.17, 3.47] 1997

Monasterolo 1998 38 150.00(16.20) 38 150.10(18.80) 7.76 -0.10 [-7.99, 7.79] 1998

Wieland 1995 39 155.00(14.00) 39 154.00(12.00) 14.43 1.00 [-4.79, 6.79] 1995

Total (95% CI) 271 271 100.00 -0.07 [-2.27, 2.13]



-10 -5 0 5 10

Decrease Increase

Fig. 4 Forest plot: effect on heart rate after skin-to-skin care, compared with that before skin-to-skin care. CI, confidence interval; SSC,skin-to-skin care; WMD, weighted mean difference.



Outcome: 03 Saturation

)dexif( DMW thgieW )dexif( DMW BeforegniruD ydutS


Acolet 1989 9 94.10(3.20) 9 94.20(2.30) 3.11 -0.10 [-2.67, 2.47] 1989

Clifford 2001 7 96.11(2.35) 7 95.92(2.70) 2.93 0.19 [-2.46, 2.84] 2001

Fohe 2000 53 93.00(3.10) 53 92.60(3.20) 14.32 0.40 [-0.80, 1.60] 2000

Huang 2002 24 96.80(1.80) 24 97.20(2.20) 15.94 -0.40 [-1.54, 0.74] 2002

Legault 1995 61 92.80(3.30) 61 94.80(2.80) 17.47 -2.00 [-3.09, -0.91] 1995

Ludington 1991 12 95.16(1.79) 12 95.79(2.02) 8.84 -0.63 [-2.16, 0.90] 1991

Ludington 2004 11 94.30(2.55) 11 95.30(1.83) 5.99 -1.00 [-2.85, 0.85] 2004

Messmer 1997 20 94.85(2.60) 20 94.85(3.40) 5.86 0.00 [-1.88, 1.88] 1997

Monasterolo 1998 38 96.40(3.30) 38 96.80(2.70) 11.21 -0.40 [-1.76, 0.96] 1998

Wieland 1995 39 93.50(2.60) 39 94.10(2.80) 14.33 -0.60 [-1.80, 0.60] 1995

Total (95% CI) 274 274 100.00 -0.60 [-1.05, -0.15]



-4 -2 0 2 4

Decrease Increase

Fig. 5 Forest plot: effect on saturation during skin-to-skin care, compared with that before skin-to-skin care. CI, confidence interval; SSC,skin-to-skin care; WMD, weighted mean difference.



https://www.researchgate.net/publication/13938724_Effect_of_kangaroo_care_on_sleep_time_for_neonates?el=1_x_8&enrichId=rgreq-746578e1-f7e1-4e7f-9f56-a5615e1a8a5f&enrichSource=Y292ZXJQYWdlOzI2Mjg1NzcxO0FTOjEwMTg5MTgxMTg0MDAwNEAxNDAxMzA0MzA5NjA4

https://www.researchgate.net/publication/13938724_Effect_of_kangaroo_care_on_sleep_time_for_neonates?el=1_x_8&enrichId=rgreq-746578e1-f7e1-4e7f-9f56-a5615e1a8a5f&enrichSource=Y292ZXJQYWdlOzI2Mjg1NzcxO0FTOjEwMTg5MTgxMTg0MDAwNEAxNDAxMzA0MzA5NjA4

Discussion

Principal results

The series of meta-analyses showed that during skin-to-skin care,there was evidence of an increase in body temperature and adecrease in oxygen saturation of babies, compared with theparameters observed before starting skin-to-skin care. Increasedbody temperature was more evident in middle–low-income set-tings than high-income settings. An increase in heart rate wasalso observed in high-income settings during skin-to-skin care.Both the positive effect on body temperature and the negativeeffect on saturation seemed to be sustained in colder environ-ments after skin-to-skin care, but there was no evidence of sucha sustained effect in a warmer environment.

The present study has a number of potential limitations in theinterpretation of these results.

Bias

There was no evidence of publication bias in the funnel plots(data not shown). All studies included only relatively stableinfants, and the results should not be applied to those withunstable conditions. All the measurements and recording of themwere conducted simultaneously; hence recall bias is unlikely.Many studies reported only the parameters for during and beforeskin-to-skin care, with no parameters for after skin-to-skin care.This can introduce selection bias, although analysis of onlystudies reporting all parameters showed a similar tendency in theresults (data not shown)

Confounding

There was a possibility of confounding by factors that have notbeen considered in the present study. Meta-regression analysisconsidered temperature of the cities where the study was con-ducted, birthweight, duration of the skin-to-skin care and the

resources of the settings. But infant age, bodyweight, and pre-maturity (term/preterm) were not reported in many of the studiesand it was therefore not possible to consider them in the presentstudy. But these parameters should have been captured by inclu-sion of birthweight in the analyses.

Measurement errors

Differences in the methods used for measuring these physiologi-cal parameters was also important. Some studies measured bodytemperature axially and other studies rectally. There could be adifference in effect, particularly the timing of warming effects.Saturation is also known to show slight variation with devicesused, as well as where in the body it was measured. But the samemeasurement method was used within the studies, and overallresults are likely to reflect the real differences. The means ofbirthweight, duration of the skin-to-skin care and resources of thesettings included in the meta-regression analyses were obtainedfrom the studies. Means may not necessarily reflect the studypopulation, although no detailed information was given. Meta-regression analyses should be interpreted with caution.

Generalizability

Studies had certain tendencies. For example, studies examiningnormal-weight infants were more likely to be conducted in high-income settings, and more likely to report only parameters beforeand during skin-to-skin care. Studies investigating babies withcongenital heart diseases and with chronic lung diseases were notconsidered in the present study. The results of the present meta-analysis should not be applied to babies other than stable normaland low-birthweight infants with no such particular conditions.

Plausibility of the effects

Human skin has a constant temperature with natural homeostasis.Therefore it is not surprising to see an increase in the body



Outcome: 03 Saturation

)dexif( DMW thgieW )dexif( DMW BeforeAfter ydutS

IC %59 % IC %59 )DS( naeMn)DS( naeMnyrogetac-bus ro

01 Temperature of the city 10 Celsius degree or lower

Wieland 1995 39 92.90(4.20) 39 94.10(2.80) 9.89 -1.20 [-2.78, 0.38]

Legault 1995 61 93.80(2.40) 61 94.80(2.80) 28.97 -1.00 [-1.93, -0.07]

Fohe 2000 53 92.30(3.00) 53 92.60(3.20) 17.79 -0.30 [-1.48, 0.88]

Subtotal (95% CI) 153 153 56.65 -0.82 [-1.48, -0.15]



02 Temperature of the city higher than 10 Celsius degree

Clifford 2001 7 96.33(2.60) 7 95.92(2.70) 3.22 0.41 [-2.37, 3.19]

Messmer 1997 20 94.85(3.40) 20 94.85(3.40) 5.59 0.00 [-2.11, 2.11]

Monasterolo 1998 38 96.90(3.10) 38 96.80(2.70) 14.52 0.10 [-1.21, 1.41]

Ludington 2004 11 94.90(2.13) 11 95.30(1.83) 9.01 -0.40 [-2.06, 1.26]

Ludington 1991 12 95.74(1.72) 12 95.79(2.02) 11.01 -0.05 [-1.55, 1.45]

Subtotal (95% CI) 88 88 43.35 -0.03 [-0.79, 0.72]



Total (95% CI) 241 241 100.00 -0.48 [-0.97, 0.02]



-4 -2 0 2 4

Decrease Increase

Fig. 6 Forest plot: effect on saturation after skin-to-skin care, compared with that before skin-to-skin care, stratified by temperature of thecities. CI, confidence interval; SSC, skin-to-skin care; WMD, weighted mean difference.

168 R Mori et al.


temperature of babies during close contact with skin. Decrease insaturation is a new finding, and reduction of saturation does notnecessarily mean apnea of prematurity, although there are oftenincreases in apnea of prematurity observed during skin-to-skincare,56 and the previous findings are compatible with the presentone. The effect is more evident in middle–low-income settings,rather than high-income settings, although there is no clear expla-nation for this. Differing levels of standard care (incubator care)to maintain temperature (e.g. faulty or old incubators, lack ofappropriate knowledge/skills etc.) may have contributed, butfurther studies to explore the findings are needed. After skin-to-skin care the effects on body temperature and saturation persistedin the colder environments. This could be due to lower baselinetemperature of babies before skin-to-skin care and effects onperipheral circulation due to the temperature of the environment,although these are speculative suggestions. One interestingfinding is that there might be an inverse relationship betweenoxygen saturation and body temperature, although this should betested in further studies. Overall, the results are biologicallyplausible, although further studies to clarify the biological cau-sation are warranted.

Implication for clinical practice

Considering the overall effects of Kangaroo Mother Care and/orskin-to-skin care in low–middle-income countries, this type ofcare can be promoted in these settings for stable low- and normal-birthweight infants. This does not imply any changes for currentconfigurations. In particular, babies at risk of apnea of prematu-rity should not given skin-to-skin care without adequate moni-toring of saturation and respiratory status. The environmentseems also to play an important role in this care. Attention shouldbe paid to ensure appropriate and adequate environment throughthe care.

Implication for research

Studies of skin-to-skin care on saturation and respiratory status ofbabies are urgently needed. Studies investigating the effect of theenvironment on the physiological status of the babies are alsoneeded. The cost-effectiveness of monitoring babies during andafter skin-to-skin care should also be thoroughly investigated invarious settings.

Conclusion

Skin-to-skin care is an effective way to warm babies, especiallywhere resources are limited and where the environment is rela-tively cold. Monitoring, however, of the saturation and respira-tory status of the babies throughout the care, where resources arerelatively affluent, should be considered, taking the costs ofmonitoring into account.

Acknowledgments

We thank all the authors of the included/excluded studies forenabling us to conduct this study. We are also grateful to Dr JacobPuliyel who reviewed this paper and provided us with valuablecomments. This study was partly supported by the grant-in-aid(health technology assessment) from the Ministry of Health,Labour and Welfare, Japan.

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Meta-analysis of physiological effects of skin-to-skin contact for newborns and mothers

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