Maternal Sensitivity in Parenting

Preterm Children: A Meta-analysis

Ayten Bilgin, MSca, Dieter Wolke, PhDa,b

Preterm birth is a signicant stressor for parents and may

BACKGROUND AND OBJECTIVES: abstract
adversely impact maternal parenting behavior. However, ndings have been inconsistent.
The objective of this meta-analysis was to determine whether mothers of preterm
children behave differently (eg, less responsive or sensitive) in their interactions
with their children after they are discharged from the hospital than mothers of term
children.
METHODS:Medline, PsychInfo, ERIC, PubMed, and Web of Science were searched from
January 1980 through May 2014 with the following keywords: premature, preterm,
low birth weight in conjunction with maternal behavio*r, mother-infant interaction,
maternal sensitivity, and parenting. Both longitudinal and cross-sectional studies that
used an observational measure of maternal parenting behavior were eligible. Study
results relating to parenting behaviors dened as sensitivity, facilitation, and
responsivity were extracted, and mean estimates were combined with random-effects
meta-analysis.
RESULTS: Thirty-four studies were included in the meta-analysis. Mothers of preterm and full-
term children did not differ signicantly from each other in terms of their behavior toward
their children (Hedges g = 20.07; 95% condence interval: 20.22 to 0.08; z = 20.94; P = .35).
The heterogeneity between studies was signicant and high (Q = 156.42; I2 = 78.9, P = .001)
and not explained by degree of prematurity, publication date, geographical area, infant age, or
type of maternal behavior.
Mothers of preterm children were not found to be less sensitive or responsive
CONCLUSIONS:
toward their children than mothers of full-term children.

a
Department of Psychology and bDivision of Mental Health and Wellbeing, Warwick Medical School, University of Warwick, Coventry, United Kingdom

Ms Bilgin conducted data collection, carried out the initial analyses, and drafted the initial manuscript; Dr Wolke conceptualized and designed the study, supervised
the study, and reviewed and revised the manuscript; and both authors approved the nal manuscript as submitted and agree to be accountable for all aspects of
the work.
www.pediatrics.org/cgi/doi/10.1542/peds.2014-3570
DOI: 10.1542/peds.2014-3570
Accepted for publication Apr 15, 2015
Address correspondence to Dieter Wolke, PhD, University of Warwick, Department of Psychology, University Road, Coventry CV4 7AL, UK. E-mail: d.wolke@warwick.ac.uk
PEDIATRICS (ISSN Numbers: Print, 0031-4005; Online, 1098-4275).
Copyright 2015 by the American Academy of Pediatrics
FINANCIAL DISCLOSURE: The authors have indicated they have no nancial relationships relevant to this article to disclose.
FUNDING: Ms Bilgin is supported by a PhD scholarship from the Republic of Turkey Ministry of Education. Dr Wolke received no funding related to this study.
POTENTIAL CONFLICT OF INTEREST: The authors have indicated they have no potential conicts of interest to disclose.

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PEDIATRICS Volume 136, number 1, July 2015 REVIEW ARTICLE
The survival rate of preterm infants
has increased rapidly as a result of the
improvements in medical and nursing
care and technology in the past
decades.1 Infants born preterm often
require care in the NICU or Special
Care Baby Units for weeks and often
months.2
Being in close contact with the
mother in the early days of life has
been proposed to be crucial for the
development of mother-infant
bonding.3 Preterm birth and
incubator care might inuence the
infant, the mother, and their
relationship. Preterm children
experience more
neurodevelopmental, cognitive, and
behavioral problems in infancy and
childhood4,5 and may be less
attentive in their communication with
their mothers,6 smile less often,7 and
be less responsive.8,9 Furthermore,
preterm birth might impair the
mothers own perception about her
ability to take care of her
newborn.10,11 Apart from separation,
this is often a stressful time for
parents because of the uncertain
outcomes for their infants. Preterm
birth has been reported to increase
the risk of depression in mothers12,13
and lead to symptoms of
posttraumatic stress disorder14 and
may adversely affect the mother-
infant relationship.1517
Maternal sensitivity has been dened
as the mothers ability to infer her
infants signals and respond to them
appropriately.18 In full-term children,
sensitive and responsive parenting
has been shown to increase cognitive,
social, and emotional outcomes.1921
On the other hand, insensitive
parenting has been related to poor
regulatory control in infancy22 and
more psychological problems in
young adulthood.23,24 Recent
evidence indicates that sensitive
parenting may be even more crucial
for preterm children to achieve
outcomes similar to full-term
children.25 Thus, increasing maternal
sensitivity and responsiveness with
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e178
interventions has been reported to
result in more developed
communication skills, improved
cognitive outcomes, and more
positive mood in preterm
infants.2628
However, there is considerable
inconsistency in ndings, with several
studies that reported mothers of
preterm infants to be as responsive or
sensitive,2931 or more so,32 than
comparison mothers. Concepts used
in observational studies of parenting
also differed and mainly referred to
sensitivity and responsiveness.33
Other than these 2 terms, behaviors
such as directiveness (statement that
directs the infant to do or say
something), suggestions (question or
statement that provides infant
a choice), and the frequency of
smiling34 were also used by some
studies. We use the term facilitation
to generally refer to these behaviors.
These inconsistencies may be due to
the children studied (ie, whether they
were born moderate to late preterm
or very preterm). In addition, better
parental access and more parental
care in recent years (after 2000) have
decreased stress for parents and
infants.35 Infant age is also a critical
factor because the differences in
maternal behavior between preterm
and full-term infants have been
suggested to lessen after 6 months of
age.30 Moreover, the differences
between the measures used to
evaluate types of parenting behavior
(sensitivity, responsivity, facilitation)
could be a critical factor to consider
in the explanation of ndings. Finally,
geographical variations in NICU care
practices (Europe versus North
America) may account for some of the
inconsistencies in the ndings
because care practices might differ
between continents.
The aim of this meta-analysis was to
systematically investigate whether
the observed maternal behavior in
interaction with their preterm infants
or children differs systematically
from that of mothers with their full-
term infants or children.
Furthermore, we investigated
whether the following factors would
moderate the results: degree of
prematurity (ie, very preterm [,32
weeks gestation] versus moderate to
late preterm birth [3236 weeks
gestation]), publication date before
2000 versus after 2000 (indicator of
recent modern NICU care and open
visiting patterns), type of parenting
behavior, and infant age and
geographical setting of the studies
(Europe or North America).
METHODS
The current meta-analysis was
conducted in line with the MOOSE
(Meta-Analysis of Observational
Studies in Epidemiology)
guidelines.36
Search Strategy
A literature search was conducted for
cross-sectional and longitudinal
studies of maternal behavior in
preterm infant-mother dyads,
published between January 1980 and
May 2014. The article search was
nalized on June 30, 2014. The
following electronic databases were
searched: Medline, PsychInfo, ERIC,
PubMed, and Web of Science. The
keywords used were as follows:
premature, preterm, low birth
weight in conjunction with maternal
behavio*r, mother-infant
interaction, maternal sensitivity,
and parenting.
The Medline search yielded 3 articles,
PsychInfo yielded 336 articles, ERIC
yielded 11 articles, PubMed yielded 70
articles, and Web of Science yielded
111 articles. Overall, 531 articles were
included in the literature search.
Forty-three duplicates were removed
from the search. Overall, the nal
literature search included 488 articles
(see Fig 1).
Study Inclusion and Exclusion
Criteria
Studies were included in the analysis
according to 5 criteria. First, articles
BILGIN and WOLKE

FIGURE 1
Flow diagram showing study eligibility.
should report on the following
maternal parenting behavior
constructs: maternal sensitivity,
which is dened as a mothers ability
to perceive and infer the meaning
behind her infants behavioral signals
and to respond to them promptly and
appropriately18; maternal
responsiveness,37,38 such as
providing stimulation to the infant; or
maternal facilitation,39,40 such as
positive regard and respect for the
childs autonomy.41 Because these
terms tapped into similar constructs,
our review used maternal parenting
behavior as an umbrella term to refer
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PEDIATRICS Volume 136, number 1, July 2015
to maternal sensitivity, maternal
responsiveness, and maternal
facilitation. Second, studies had to use
an observational instrument to
measure maternal parenting behavior.
Third, studies had to include a full-
term comparison group. Fourth,
enough statistical information
(correlations, means, and SDs; sample
size; P or t values) should be reported
in the articles or provided by authors
after contacting them to enable
computing effect sizes. Last, the
articles had to be in English. Studies
not fullling these criteria were
excluded (Fig 1).
The titles and abstracts of 488
articles were reviewed, and 293 were
excluded on the basis of the abstract
only. We reviewed the full text of the
remaining 195 articles according to
the inclusion criteria, and 155 articles
were excluded. Furthermore, 6
studies had no information to
compute effect sizes. The contact
information of one of the authors42
could not be found. The other authors
of these studies were contacted;
however, 3 of the authors did not
reply4345 and 2 could not provide
the information.17,34 Thirty-four
studies were included in the meta-
analysis (Table 1). The article
selection process was performed by
Ayten Bilgin and Hayley Boulton
independently. The overall agreement
in the selection of articles according
to the predened criteria was Cohens
k 0.86 at the abstract selection stage
and 0.83 at the full-text retrieval
stage. The discrepancies in 10 articles
were discussed and mutually
resolved by the coders.
Quality Assessment
The Newcastle-Ottawa Scale was used
to assess the quality of studies
referring to selection, comparability,
and outcome or exposure for case-
control and cohort studies (see
Supplemental Tables 2 and 3). Scores
in this scale could range from 0 to 9,
with higher scores indicating higher
quality. Studies were rated by 2
independent coders, and agreement
for the overall rating for each study
was found to be high (k = 0.82). The
overall ratings of the studies ranged
from 7 to 9 (mean = 8.08, SD = 0.79),
indicating overall high quality.
Data Extraction
Eligible studies were reviewed to
extract the observed maternal
behavioral data. When available,
information on the comparison of
preterm and full-term groups was
extracted directly from the article.
Different studies provided the data in
different formats: sample size with
means and SDs, P value, or t value.
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 TABLE 1 Summary of the Studies Included in the Analysis

e180
Study N Age Birth Weight, Mean Gestational Age, Mean Gender (Male/ Design Duration of Instrument Result Moderators
(SD), Range g1 (SD), Range, wk1 Female), n Observation
Type of Parenting Degree of Publication Geographical Infant
Behavior Prematurity Date Setting Age
Agostini et al46 P: 69; 3 mo P: 1040.71 (127.49); P: 28.53 (1.7); P: 45/24; F: 42/38 CS 5 min Global rating NS Maternal VPT After 2000 Europe #6 mo
F: 60 F: 3410.24 F: 39.86 (1.13) scales47: 5-point sensitivity
(462.76) scale to rate
sensitivity,
intrusiveness,
remoteness, signs
of depression
Barnard et al39 P: 88; 4, 8, and No information P: #34, 31.1 (1.45); F: P: 40/48; F: 83/83 LN 1 to 2 h 4-point scale to rate S/S/S Maternal VPT Before North America .6 mo
F: 166 24 mo 39.4 (1.1) maternal facilitation 2000
responsiveness to
infants distress or
satiation cues
Barratt et al37 P: 24; 4 mo P: 14602420 (mean P: 3136 (mean = 34); No information CS 1 h, 10 min Initiations of the S Maternal M/LPT Before North America #6 mo
F: 24 = 2099); F: 2849 F: 3742 (mean = following behaviors responsiveness 2000
to 4408 (mean = 40) were coded:
3493) mother
vocalizations,
touches, and
smiles
Barratt et al48 P: 21; 12 and P: 14602420 (mean P: 3136 (mean = 34); P: 8/13; F: 8/13 LN 90 min Coded behaviors: NS/S Maternal M/LPT Before North America .6 mo
F: 21 20 mo = 2125); F: 3843 (mean = manual directives, responsiveness 2000
F: 28924253 40) manual assistance,
(mean = 3505) intrusion in the
toddlers play,
demonstration of
object properties,
object exchanges,
smiles, looking
Bendersky and P: 31; 3 mo P: 1615.3 P: 32.2 (2637); No information CS 15 mins A checklist developed NS Maternal M/LPT Before North America #6 mo
Lewis49 F: 28 (7092180); F: 40.14 (3942) by Lewis and Lee- responsiveness 2000
F: 3587.9 Painter50;

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(26084564) responsiveness
was conceptualized
as the amount of
behavior that
involves response
to the infant
Coppola et al51 P: 20; 3 mo P: 1201.25 (166.2); P: 29.9 (2.6); 18/22 CS 10 min Parental sensitivity NS Maternal VPT After 2000 Europe #6 mo
F: 20 F: 3368 (445.5) F: 38.9 (0.8) items from sensitivity
Emotional
Availability Scale52

BILGIN and WOLKE

 TABLE 1 Continued
Study N Age Birth Weight, Mean Gestational Age, Mean Gender (Male/ Design Duration of Instrument Result Moderators
(SD), Range g1 (SD), Range, wk1 Female), n Observation
Type of Parenting Degree of Publication Geographical Infant
Behavior Prematurity Date Setting Age
Crawford53 P: 16; 6, 8, 10, P: 1287 (6601850); P: 29.6 (2433); No information LN 10 min The frequency of the S/S/S/NS Maternal VPT Before North America .6 mo
F: 17 and F: 3242 (2610 F: 39.6 (3842) following facilitation 2000
14 mo 3740) behaviors: holding
the infant,
attending to the
needs of the infant,
affectionate kissing
or hugging, talking
to infant

PEDIATRICS Volume 136, number 1, July 2015

Davis and P: 10; 2,3,4,and P: 1520 P: 31 (2835); F: 40 P: 5/5; F: 17/12 LN 7h Frequency of the S Maternal M/LPT Before North America #6 mo
Thoman54 F: 29 5 wk (12602100); (3742) following facilitation 2000
F: 3536 behaviors: move,
(27504395) rock, pat, caress,
talk, look, vis-a-vis
(eye to eye
contact), hold/
carry, smile/laugh,
suck/stimulate
DeWitt et al55 P: 115; 6 and P: 1072.5; F: 3111 P: 29.2; F: 39.7 P: 51/64; F: 52/53 LN 70 min 5-point rating scale S Maternal VPT Before North America .6 mo
F: 105 12 mo based on sensitivity 2000
Ainsworth56 and
Crockenberg 57
Feldman and P: 56; Term, P: 1278.1 (234.1); P: 30.38 (2.5); P: 30/26; F: 29/23 LN 15 min at At term coded by the S/NS Maternal VPT After 2000 Europe #6 mo
Eidelman58 F: 52 3 mo F: 3321 (457.1) F: 38.82 (2.98) term, 90 Mother-Newborn facilitation
min at Coding System of
3 mo the Coding
Interaction
Behavior
Manual59; at 3 mo
HOME60 and
a microanalytic

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computerized
coding system
Forcada-Guex P: 47; 6 and No information P: ,34, 31 (2); P: 22/25; F: 10/15 LN 10 min Third revision of Care S Maternal M/LPT After 2000 Europe #6 mo
et al61,a F: 25 18 mo F: $37, 40 (1) Index62 assesses 3 sensitivity
scales: sensitivity,
control, and
unresponsiveness
Greenberg and P: 30; 24 mo P: 1407 (8401800); P: 31 (2736); F: 40 P: 17/13; F: 17/23 CS 10 min Ratings were on the NS Maternal M/LPT Before North America .6 mo
Crnic63 F: 40 F: 3521 (3942) following facilitation 2000
(28604520) behaviors:
gratication from
the interaction,
general affective
tone, sensitivity to
infant cues

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 TABLE 1 Continued

e182
Study N Age Birth Weight, Mean Gestational Age, Mean Gender (Male/ Design Duration of Instrument Result Moderators
(SD), Range g1 (SD), Range, wk1 Female), n Observation
Type of Parenting Degree of Publication Geographical Infant
Behavior Prematurity Date Setting Age
Greene et al64 P: 30; 3 mo P: 1642 (303); P: 32.8 (2.4); F: 40 P:15/15; F:16/16 CS 15 min Checklist sheet S Maternal M/LPT Before North America #6 mo
F: 32 F: 3518.5 (588.5) (1.2) developed by Lewis facilitation 2000
and Lee-Painter50;
frequency of the
following maternal
behaviors was
rated: (1) touch, (2)
hold, (3)
vocalization to
infant (vocalization
to other category
omitted), (4) look,
(5) smile/laugh, (6)
play with infant, (7)
change diaper/
bathe (wash his/
her hands, face),
(8) feed (includes
breast, bottle,
spoon), (9) rocks
subject, (10) read,
(11) kiss, and (12)
give toy/pacier
Halpern and P: 20; 4 mo P: 1673.3; F: 3421.3 P: 32.8 (2836); No information CS 15 min 12-item rating scale66 NS Maternal VPT Before North America #6 mo
McLean65 F: 20 F: 40 (3843) that rated facilitation 2000
supportiveness,
patience,
expression of
positive and
negative feelings,
responsivity,

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behavioral
repertoire
Jaekel et al9 P: 267; 6 y, 3 mol P: 1296 (308); P: 30.4 (2.3); F: 39.6 P: 143/124; LN 12 min A standardized coding S/S Maternal VPT After 2000 Europe .6 mo
F: 298 8 y, F: 3388 (450) (1.2) F: 152/146 system, sensitivity
5 mo Assessment of
Mother-Child
Interaction with the
Etch A Sketch67
Jean and P: 40; 5 mo P: 1092 (237); P: 28.5 (2.3); F: 39.74 P: 18/22; F: 20/20 CS 6 min Sensitivity scale of S Maternal VPT After 2000 North America #6 mo
Stack68 F: 40 F: 3476 (395) (1.08) Emotional sensitivity
Availability scale52
Korja et al29 P: 32; 6 and P: 1008 (289); P: 28 (3); F: 40 (1) P: 19/13; F: 19/17 LN 5 min Parent-Child Early NS/NS Maternal VPT After 2000 Europe .6 mo
F: 36 12 mo F: 3589 (406) Relational facilitation
Assessment,69
5-point Likert scale

BILGIN and WOLKE

 TABLE 1 Continued
Study N Age Birth Weight, Mean Gestational Age, Mean Gender (Male/ Design Duration of Instrument Result Moderators
(SD), Range g1 (SD), Range, wk1 Female), n Observation
Type of Parenting Degree of Publication Geographical Infant
Behavior Prematurity Date Setting Age
Landry et al70 P: 48; 36 mo P: 1258.5 (283); P: 30.4 (2.11); P: 25/23; F: 12/9 CS 20 min Frequency of the S Maternal VPT Before North America .6 mo
F: 21 F: 3200 (760) F: 41 (2.1) following facilitation 2000
behaviors:
directives,
suggestions,
restrictions, praise
Laucht et al71 P: 119; 3 mo P: 1625.5 (229.5); P: 33 (2.3); F: 39.4 171/176 CS 10 min Mannheim rating NS Maternal VPT After 2000 Europe #6 mo
F: 228 F: 3274 (419) (1.7) system72 sensitivity
Levy-Shiff and P: 38; 2, 3, and P: 1254 (375); P: 30 (3.2); F: 41 (0.8) P: 19/19; F: 19/19 LN 30 min Behaviors coded: S Maternal M/LPT Before Europe #6 mo

PEDIATRICS Volume 136, number 1, July 2015

Mogilner73 F: 38 4 wk F: 3510 (450) caregiving, talking, facilitation 2000
playing and
stimulating,
expressing positive
affection, holding,
looking
Miljkovitch P: 48; 6 and No information P: ,33; F: .37 No information LN 5 min Ainsworth Maternal S/NS Maternal VPT After 2000 Europe .6 mo
et al74 F: 23 18 mo Sensitivity Scale56 sensitivity
and the Care
Index,62 which
codes the following
behaviors:
sensitivity,
controlling,
unresponsive
Minde et al75 P: 20; 1, 2, and P: 1124 (173); P: 2632 P: 10/10; F: 8/12 LN 10 min Frequency and S/S/S Maternal VPT Before North America #6 mo
F: 20 3 mo F: 3196 (326) duration of the facilitation 2000
following
behaviors: look,
verbalize, touch,
hold, nipple in
mouth

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Montirosso P: 25; 9 mo P: 1516 (483), P: 32.1 (2.8), 2636; F: P: 14/11; F: 13/12 CS 6 min Infant and caregiver NS Maternal M/LPT After 2000 Europe .6 mo
et al30 F: 25 8452450; F: 3293 39.9 (1.2), 3741 engagement facilitation
(382), 25403840 phases76
Muller-Nix P: 47; 6 and No information P: 31 (2); F: 40 (1) P: 22/25; F: 10/15 LN 10 min Third revision of Care S/S Maternal M/LPT After 2000 Europe .6 mo
et al15,a F: 25 18 mo Index62 assesses 3 sensitivity
scales: sensitivity,
control, and
unresponsiveness

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 TABLE 1 Continued

e184
Study N Age Birth Weight, Mean Gestational Age, Mean Gender (Male/ Design Duration of Instrument Result Moderators
(SD), Range g1 (SD), Range, wk1 Female), n Observation
Type of Parenting Degree of Publication Geographical Infant
Behavior Prematurity Date Setting Age
Potharst et al41 P: 94; 5y P: ,1000; F: .2500 P: ,30; F: .37 No information CS 15 min The NICHD (2003) Early S Maternal VPT After 2000 Europe .6 mo
F: 84 Child Care facilitation
Research Network
coding system,77
which measure
mothers
supportive
presence and
respect for the
childs autonomy
Rahkonen P: 48; 2y P: 876 (194); F: 3613 P: 26.3 (1.2); F: 40.2 P: 31/17; F: 11/5 CS 15 min Mutually responsive NS Maternal VPT After 2000 Europe .6 mo
et al31 F: 16 (354) (0.9) orientation78 and sensitivity
quality of
relationship79
Schermann- P: 142; 2, 4, and P: 1829.5 (440); P: 31.4 (1.7); F: 39.7 P: 58/84; F: 29/41 LN 5 min Behaviors rated on NS/NS/ Maternal VPT Before Europe #6 mo
Eizirik80 F: 70 6 mo F: 3558 (409) (1.1) a 5-point scale NS sensitivity 2000
were sensitivity,
intrusiveness, and
involvement
Schmcker P: 79; 3 mo P: 938.3 (288.4); P: 27.5 (2.7); F: 39 P: 36/43; F: 12/22 CS 10 min Microanalytic coding S Maternal VPT After 2000 Europe #6 mo
et al33 F: 35 F: 3333 (400.3) (1.2) system of mother- responsiveness
infant
interaction81
Singer et al82 P: 171; 8 and P: 1111 (205.5); P: 28.8 (2); F: 39.8 (1) P: 79/92; F: 58/50 LN No information The Nursing Child NS/NS Maternal VPT After 2000 America .6 mo
F: 117 12 mo F: 3463 (520) Assessment sensitivity
Feeding Scale83
Stevenson P: 17; 8 mo P: 2140 (216); P: 34.1 (1.3); F: 39.9 P: 8/9; F: 8/9 CS 10 min Onset and offset of the S Maternal M/LPT Before America .6 mo
et al38 F: 17 F: 3509 (464) (1.6) following behaviors facilitation 2000
were recorded:
proffer food,
vocalize, look

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toward, touch
infant, smile,
present objects
Watt and P: 14; 2 and No information P: 33.1 (3135) No information LN P: 32.4 Frequency of the NS/S Maternal M/LPT Before Europe #6 mo
Strongman84 F: 10 3 mo (21.843) following behaviors facilitation 2000
min; F: 34.7 were recorded:
(19.847.6) vocalize, look,
min smile, kiss, hug,
rock, tickle,
affectionate touch,
play
Wille85 P: 36; 6 mo P: 1929.5 (353); P: 34 (1.5); F: 40 (1) P: 19/17; F: 9/9 CS 15 min Second-by-second S Maternal M/LPT Before America #6 mo
F: 18 F: 3495 (218) monadic phase facilitation 2000
system86

BILGIN and WOLKE

 TABLE 1 Continued
Study N Age Birth Weight, Mean Gestational Age, Mean Gender (Male/ Design Duration of Instrument Result Moderators
(SD), Range g1 (SD), Range, wk1 Female), n Observation
Type of Parenting Degree of Publication Geographical Infant
Behavior Prematurity Date Setting Age
Wolke et al87 P: 90; Term, P: 1245 (5212158); P: 30 (2433); F: 39 P: 51/39; F: 63/52 LN 3 min Mother-Infant S/NS Maternal VPT After 2000 Europe #6 mo
F: 115 3 mo F: 3170 (3742) Structured Play sensitivity
(18204380) Instrument, 5-point
scale of maternal
positive emotional
expression,
sensitivity,
stimulation level
adapted from

PEDIATRICS Volume 136, number 1, July 2015

Emotional
Availability Scales88
and Infant and
Caregiver
Engagement
Phases89
Zarling et al8 P: 34; 6 mo P: 1243 (218); P: 30 (2); F: 3040 P: 51/39; F: 63/52 CS 5 min 5-point scale that S Maternal VPT Before America #6 mo
F: 30 F: .2500 measures the sensitivity 2000
reciprocity,
intrusiveness,
responsiveness,
affect,
successfulness
with infant,
appropriateness of
verbal and
nonverbal
techniques
1Mean, SD, and range values are reported if available. CS, cross-sectional; F, full-term; HOME, Home Observation for Measurement of the Environment; LN, longitudinal; M/LPT, moderate to late preterm; P, preterm; NICHD, Eunice Kennedy Shriver
National Institute of Child Health and Human Development; NS, no signicant difference; S, signicant difference; VPT, very preterm.
a These 2 studies reported ndings from the same sample. We used the 18-month data from the Muller-Nix et al study and the 6-month data from the Forcada-Guex et al study.

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e185
When any of this information was
unavailable, it was requested from
the authors. In cases in which the
researchers reported the statistical
information for each observed
maternal behavior separately, a mean
score and a pooled SD score were
computed. Furthermore, categorical
information regarding the degree of
prematurity, publication before or
after 2000, geographical setting, type
of parenting, and infant age was
extracted from the articles (Table 1).
Furthermore, type of parenting
behavior was coded as maternal
sensitivity or responsivity in
accordance with what was reported
in the Results section. Facilitation was
coded when maternal behaviors were
reported separately without being
referred to as sensitivity or
responsiveness. One exception was
Barnard et al,39 which was coded as
facilitation, even though responsivity
was also reported in the study,
because facilitation was reported at
all measurement times. The
categorization of these variables was
completed by the rst author (A.B.)
under the supervision of the second
author (D.W.).
Data Analysis
Analysis was conducted with
Comprehensive Meta-Analysis
version 2 software.91 All studies
provided continuous measures of
observed maternal parenting
behavior, comparing preterm and full-
term control samples. Mean effect
sizes were calculated with the
Comprehensive Meta-Analysis
software when studies reported
group differences at different time
points. A random-effects model was
used to generate the combined
estimate of the effects (Hedges g).
Random-effects models take into
account that effect sizes will differ
from 1 study to another because they
are sampled from an unknown
distribution.47 Heterogeneity of
studies was assessed with Cochrans
Q and Higgins I2. Moderator analyses
were conducted with 5 variables:
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e186
degree of prematurity, publication
before or after 2000, geographical
setting, infant age, and type of
parenting behavior. Sensitivity
analysis was undertaken with the
outlier.
Publication bias analysis was
assessed as follows:
1. Rosenthals fail-safe number92,93
was used to address the le-
drawer problem. Rosenthals fail-
safe number test produces the
number of unpublished studies
needed to bring the combined ef-
fect size to a statistically non-
signicant level. Publication bias
does not exist if Rosenthals fail-
safe number exceeds 5k + 10,
where k is the number of studies
used in meta-analysis.
2. The trim and ll procedure94 was
used to examine the symmetry of
effect sizes plotted by the inverse
of the SE. Ideally, the effect sizes
should mirror one another on ei-
ther side of the mean.
3. The Begg and Mazumdar rank
correlation test95 was used to ex-
amine the likelihood of bias in fa-
vor of small sample size studies.
Nonsignicance of correlation
indicates no publication bias.
4. Eggers test96 examined whether
publication bias related to the di-
rection of study ndings. The in-
tercept value provided by this test
shows the level of funnel plot
asymmetry from the standard
precision.
RESULTS
The 34 studies included a total of
3905 participants, 1981 preterm and
1924 full-term comparison children.
Thirteen of the studies investigated
moderate to late preterm (3236
weeks gestation) and 21 studies
reported on very preterm children
(,32 weeks gestation). Mean birth
weight was 1374 g (SD = 234 g) for
the preterm participants and 3450 g
(SD = 545 g) for the full-term
participants. The mean gestational
age of the preterm children was 30.4
weeks (SD = 2.2 weeks) compared
with 39.8 weeks (SD = 1.1 week) for
the full-term comparisons. Fifty
percent (n = 17) of the studies were
longitudinal (ie, had .1 assessment
point). Four of the studies reported
on observed maternal responsivity
(12%), 14 on observed maternal
sensitivity (41%), and the rest
described observed mother behavior
as maternal facilitation (47%). The
overall sample size of the studies
ranged from 33 to 565 (median = 71).
The mean age of the participants
included in the studies was 13.9
months (median = 6 months). Twenty-
one of the studies included
participants ,12 months, with a mean
age of 4 months (range: 2 weeks to 9
months). The other 13 studies
included participants aged $12
months (mean = 28.07 months; range:
12 months to 8 years, 5 months).
The combined mean effect size of
observed maternal parenting
behavior was Hedges g = 20.07
(95% condence interval: 20.22 to
0.08; z = 20.94; P = .35), indicating
no difference in the parenting
behavior of mothers of preterm and
full-term comparison children.
Heterogeneity analysis indicated
signicant and high variation in
effects between studies (Q = 156.42;
I2 = 78.9, P = .001) (Fig 2).
Moderator Analysis
Planned moderator analysis revealed
that the degree of prematurity was
not a signicant moderator (Q = 0.02,
P = .88) (see Supplemental Fig 4).
Being published before or after 2000
was also not a signicant moderator
for the main analysis (Q = 1.47, P =
.23) (see Supplemental Fig 5), nor
was whether the studies were carried
out in North America or Europe (Q =
0.77, P = .38) (see Supplemental
Fig 6). Similarly, infant age (Q = 0.01,
P = .92) (see Supplemental Fig 7) and
the type of observed maternal
parenting behavior did not moderate
the ndings (Q = 2.76, P = .25) (see
Supplemental Fig 8).
BILGIN and WOLKE
FIGURE 2
Difference between preterm and full-term mother infant dyads. CI, condence interval. Favors A, Favors full-term infants; Favors B, favors preterm infants
Outliers and Sensitivity Analysis
Outliers are dened as studies that
had signicantly different effect sizes
from the other studies.97 One study61
was identied as an outlier because it
had substantially higher effect sizes
than the other studies. As suggested
by Borenstein et al,97 we repeated the
meta-analysis excluding the outlier to
check whether this result altered the
combined effect size and reduced
heterogeneity. Results remained
nonsignicant when the outlier was
removed from the analysis (Hedges
g = 20.02, P = .76) (Fig 3) and the
level of heterogeneity decreased (Q =
103.07; I2 = 68.95, P = .001).
Publication Bias
The fail-safe number addresses the
concern that the observed differences
may be false and was not relevant in
the current study because the
combined result did not indicate
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PEDIATRICS Volume 136, number 1, July 2015
group differences. Under the random-
effects model, the point estimate
(95% condence interval) for the
combined studies is 20.097 (20.33
to 0.13). With the use of trim and ll,
these values remained unchanged,
indicating no publication bias.
Furthermore, the Begg and
Mazumdar rank correlation was not
signicant and Eggers test was not
statistically signicant, indicating no
evidence of publication bias.
DISCUSSION
Meta-analysis revealed no evidence of
differences in mothers observed
parenting behavior with their
preterm infants or children compared
with mothers of full-term
comparisons. The ndings did not
alter signicantly when moderators
such as degree of prematurity,
geographical location, infant age, type
of parenting behavior, or time of
neonatal care (before or after the
2000) were considered. Furthermore,
excluding the outlier did not alter the
ndings and the results cannot be
accounted for by publication bias.
Mothers of preterm children
repeatedly have been described at
risk of being less sensitive in their
interactions with their infants.45,98 It
has been proposed that mothers
ability to respond to their preterm
infants needs appropriately might be
negatively affected by long-term
incubator care3,99,100 or by mothers
high levels of stress.15 Nevertheless,
the results from our meta-analysis
indicate that mothers of preterm
children provide, on average, similar
observed sensitive and responsive
parenting for their preterm offspring
as mothers with a full-term infant.
This nding provides support to the
studies that reported similar levels of
e187
FIGURE 3
Difference between preterm and full-term mother infant dyads- Without outlier. CI, condence interval. Favors A, Favors full-term infants; Favors B, favors
preterm infants
observed maternal behavior in
preterm and full-term infants during
the rst year of life.29,30,46,63,80
Maternal sensitivity has been
previously reported to be a predictor
of the development of secure infant-to-
mother attachment.101 In preterm
infants, maternal sensitivity has been
linked to positive developmental
outcomes,102 whereas insensitivity has
been found to increase impairments in
self-regulation.103 Similar outcomes
in preterm infants were also observed
when maternal responsivity and
facilitation were measured.43,84,104 We
carefully distinguished between the
different maternal parenting
behaviors: sensitivity, responsivity, and
facilitation. This method allowed us to
examine the impact of all parenting
behavior as well as the moderating
role of using different constructs in
analysis. Nevertheless, type of
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e188
parenting did not make a difference in
the outcome, which suggests that our
ndings are generalizable across these
different maternal parenting behaviors.
Increased levels of maternal
stimulation and intrusiveness have
been associated with negative
outcomes.105 However, Wijnroks106
showed that intrusive parenting did
not lead to negative outcomes in
preterm children. On the contrary,
preterm children were found to have
better cognitive outcomes and better
ability to sustain attention at the age
of 2 years. Similarly, Jaekel et al25 and
Eryigit Madzwamuse et al107
reported that differences in parenting
behavior disappeared once
intellectual abilities of the infants/
children were controlled for. Thus,
children who were delayed and had
lower IQ scores may need more
framing and directive parenting,
which may be considered as intrusive
in normally developing children.
Knowing that preterm children are
more likely to have developmental
delay, our nding of no differences in
observed parenting is even more
remarkable.
Evidence from some recent studies
suggests that differences between
preterm and full-term infants in
observed maternal behavior may
decrease after the rst 6 months.28,29
In this meta-analysis, 19 studies
included infants aged #6 months and
15 studies included children aged $7
months. No impact of infant age on
maternal observed behavior was
found in moderator analysis.
Previous research considered the
length of stay in hospital and the
degree of neonatal illness as
important predictors of the
BILGIN and WOLKE
socioemotional development of
preterm infants.108 Increased
neonatal morbidity and prolonged
hospital stay may adversely shape the
quality of the relationship between
the mother and infant.109 Very
preterm infants experience, on
average, more neonatal complications
and interventions and longer hospital
stay than moderate to late preterm
infants.110 However, no difference in
observed parenting behavior of
mothers of very preterm versus
moderate to late preterm infants was
found in the current meta-analysis.
This nding provides no evidence for
the suggestion that lower gestational
age, often associated with longer
hospitalization, adversely affects
observed maternal parenting and is in
line with studies that directly
explored the impact of severity of
neonatal illness43 or birth weight on
maternal parenting behavior.71
Alleviating maternal stress by early
intervention has been shown to
increase the amount of sensitivity of
mothers of preterm infants at 12
months.27 Recent improvements in
neonatal support were proposed to
have led to more involved care and
improved interaction during initial
hospitalization.29 Practices in NICU
care regarding parent involvement
started changing in the 1990s but
have varied widely between units
within and between countries. We
used the year 2000 as an
approximation cutoff point to
distinguish between less and more
family-centered care. European NICUs,
in particular the United Kingdom,
implemented parental 24-hour visiting
routinely in the 1980/1990s, whereas
this practice appears to have been
later in many North American NICUs.
However, our moderator analyses did
not show a signicant effect of studies
being conducted before or after 2000
or of being conducted in Europe or
North America.
The nding that preterm and full-
term mothers do not differ in their
observed parenting behavior is highly
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PEDIATRICS Volume 136, number 1, July 2015
reassuring for health professionals
and parents. The stress of having
a preterm child has been often
considered to adversely affect
parenting behavior and long-term
development.111 Nevertheless, our
ndings indicate considerable
resiliency in observed parenting
behavior. New longitudinal research
indicates that preterm children may
need increased sensitive and
facilitative parenting to scaffold their
behavior to deal with tasks and
emotional regulation.25 This
approach may include more guided
and directive behavior.17,46,64
Furthermore, the nding that preterm
infants are more inuenced by low-
or high-sensitive parenting suggests
more susceptibility to parenting.48
Thus, we speculate that mothers of
preterm children may need to be even
more responsive and facilitative than
mothers of full-term children for their
children to reach the same potential.
Strengths and Limitations
Our studys strengths are that we
included only studies that had direct
observations of maternal parenting
behavior with usually high
interobserver reliability. We excluded
studies that used self-report
questionnaires of maternal parenting
behavior. Direct observations provide
only a short window into maternal
parenting behavior, whereas maternal
reports of behavior refer to longer
periods but may often be inuenced
by maternal factors such as
depression.112 Furthermore, the use
of expert observations, veried by
interobserver agreement, is less likely
to be biased by previous experiences
and mental state than maternal
reports of parenting.
A limitation is that the current meta-
analysis included only articles
published in English. We cannot be
certain whether this may have
introduced bias. However, for the
studies analyzed here and published
in the English language no indication
of publication bias was found.
Furthermore, heterogeneity was high,
indicating considerable variation
between studies. This heterogeneity
might arise from incorporating
studies that have various designs and
sample sizes. To address this
possibility, we used random-effects
model in the analysis and conducted
moderator analysis with potential
variables. However, the predened
moderator variables could not explain
the heterogeneity between studies
and additional moderators may be
considered in future research. Major
heterogeneity may arise by the use of
a wide range of observation methods.
However, we could not test this
possibility because measures differed
from one study to another. Moreover,
we used the year 2000 as an articial
cutoff point, which is a convenient
approximation of changed NICU care
(visiting patterns) and might not
represent the exact time for the
improvements in the NICUs included
in the meta-analysis. Finally, we
computed mean scores if the study
reported observations of maternal
behavior over several time points.
Therefore, longitudinal changes were
not addressed in the current analysis
but may be of interest in future. The
inuence of specic medical
complications on any potential
differences between mothers of
preterm and full-term infants could
not be addressed. Very few studies
provided information on medical
complications and thus could not be
considered as a moderator. However,
it is critical for future studies to
consider the level of medical
complications in preterm infants
when studying mothers behavior.
Conclusions
Despite being born preterm and often
spending weeks or months in
neonatal care, mothers observed
parenting behavior in interaction
with their preterm children was not
found to be less sensitive, facilitative,
or responsive than that of mothers of
full-term children. The ndings
provide reason for optimism that
most mothers, despite their initial
e189
shock and stress and the challenges of
dealing with a preterm infant, show
sensitive and responsive behavior
that is comparable to mothers of full-
term children. However, whether
these similar levels of observed
maternal behavior are sufcient or
appropriate to foster optimal
development of preterm children
requires further longitudinal
investigation.24,25
ACKNOWLEDGMENT
We thank Dr Hayley Boulton, PhD, for
her contributions to the study.
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 Maternal Sensitivity in Parenting Preterm Children: A Meta-analysis
Ayten Bilgin and Dieter Wolke
Pediatrics 2015;136;e177; originally published online June 1, 2015;
DOI: 10.1542/peds.2014-3570
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PEDIATRICS is the official journal of the American Academy of Pediatrics. A monthly

publication, it has been published continuously since 1948. PEDIATRICS is owned, published,
and trademarked by the American Academy of Pediatrics, 141 Northwest Point Boulevard, Elk
Grove Village, Illinois, 60007. Copyright 2015 by the American Academy of Pediatrics. All
rights reserved. Print ISSN: 0031-4005. Online ISSN: 1098-4275.

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 Maternal Sensitivity in Parenting Preterm Children: A Meta-analysis
Ayten Bilgin and Dieter Wolke
Pediatrics 2015;136;e177; originally published online June 1, 2015;
DOI: 10.1542/peds.2014-3570

The online version of this article, along with updated information and services, is
located on the World Wide Web at:
/content/136/1/e177.full.html

PEDIATRICS is the official journal of the American Academy of Pediatrics. A monthly

publication, it has been published continuously since 1948. PEDIATRICS is owned,
published, and trademarked by the American Academy of Pediatrics, 141 Northwest Point
Boulevard, Elk Grove Village, Illinois, 60007. Copyright 2015 by the American Academy
of Pediatrics. All rights reserved. Print ISSN: 0031-4005. Online ISSN: 1098-4275.

Downloaded from by guest on November 18, 2016