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Infancy - 2022 - Lev Enacab - Spontaneous Movements Motor Milestones and Temperament of Preterm Born Infants
Infancy - 2022 - Lev Enacab - Spontaneous Movements Motor Milestones and Temperament of Preterm Born Infants
DOI: 10.1111/infa.12451
RESEARCH ARTICLE
1
Maccabi Health Care Service, Haifa,
Israel Abstract
2
University of Haifa, Haifa, Israel Preterm-born infants and their mothers are at higher
3
Medical University of Graz, Graz, risk of showing less attuned interactions. We sought
Austria to identify characteristics of preterm-born infants as-
sociated with the attunement of mother–infant inter-
Correspondence
Orna Lev-Enacab, Maccabi Health Care actions at the corrected ages of 3–4 months, looking
Service and University of Haifa, Haifa, specifically at motor behaviors. We focused on infants’
Israel.
Email: levorna26@gmail.com
spontaneous movements, achievement of motor mile-
stones, and temperament, which at this young age is
Funding information often manifested via movement. Sixty preterm-born in-
Faculty of Social Sciences, University
of Haifa; Maccabi Health Care Service; fants (Mdngestation age in weeks = 33, 57.38% male, corrected
Israeli Physiotherapy Society age Mdn = 14 weeks, interquartile range = 13–16) and
their mothers participated. Independent observers rated
mother–infant attunement, infants’ spontaneous move-
ments, and infants’ achievement of motor milestones.
Mothers reported infant temperament. We found in-
fants’ smooth and fluent movement character and con-
tinual fidgety movements were associated with better
attunement in terms of higher maternal sensitivity and
non-intrusiveness and higher infant responsiveness and
involvement. Unexpectedly, infants’ achievement of
motor milestones was not significantly associated with
mother–infant attunement, and maternal reports of in-
fants’ higher soothability were associated with lower
| wileyonlinelibrary.com/journal/infa
412 Infancy. 2022;27:412–432.
LEV-ENACAB et al. | 413
1 | I N T RO DU CT ION
During the first six months of life, preterm-born infants are at risk of experiencing poorer quality
of interactions with their mothers, which puts the infants at risk of poorer socio-emotional and
cognitive development (e.g., Gueron-Sela et al., 2015; Korja et al., 2012). Certain behavioral char-
acteristics of preterm-born infants may contribute to difficulties in mother–infant interactions.
The present study examined three potentially relevant characteristics of infants at the corrected
ages (CA) of 3–4 months that involve motor behaviors: (1) atypical or abnormal spontaneous
movements, such as vigorous arching of the body; (2) slower achievement of gross motor mile-
stones; and (3) more difficult temperament. We assessed the latter because movement is a key
modality through which temperament is expressed at this young age (Planalp et al., 2017). Studies
have shown that all three are more prevalent among preterm- than term-born infants (Di Rosa
et al., 2016; Fjørtoft et al., 2016; although the evidence regarding temperament is less consistent;
Cassiano et al., 2020). To the best of our knowledge, research on the associations between the
characteristics of spontaneous movements and the quality of the interactions between infants
born preterm and their mothers is scarce (Lev-Enacab et al., 2015). In addition, the few studies
examining the contributions of the achievement of gross motor milestones or of temperament
to the quality of mother–infant interactions have reported mixed results (e.g., White-Traut et al.,
2018, versus Treyvaud et al., 2009; Feldman, 2006, versus Harel-Gadassi et al., 2020).
Researchers have offered several closely related constructs to characterize the quality of mother–
infant interactions. Here, we use the term attunement, a dyadic construct reflecting reciprocal
multilevel behaviors of the mother and the infant (Bornstein, 2013). Maternal attunement in-
volves sensitive behaviors (Bartling et al., 2010; Bornstein, 2013), namely being attentive to the
infant's cues, interpreting them accurately, and responding to them appropriately and in a timely
manner (Ainsworth, 1969). Sensitive mothers show positive affect, warm concern, and social
responsiveness to their infants’ needs (Bartling et al., 2010; Bornstein, 2013) without intrusive-
ness, i.e., without interfering, overstimulating, or overprotecting the infant (Biringen et al., 2014;
Bornstein, 2013). Infants contribute to attunement by being engaged with their mothers, signal-
ing their needs, responding positively to their mothers’ bids, and initiating interactions (Biringen
et al., 2014; Bornstein, 2013).
Mother–infant attunement fosters infants’ exploration and quick recovery from distress
(Ainsworth, 1969; Bornstein, 2013). It predicts better developmental outcomes of full-term
and preterm infants alike, including forming secure attachment, showing better cognitive
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414 LEV-ENACAB et al.
development and language skills in toddlerhood, and displaying higher social competence and
fewer behavior problems in early and late childhood (Biringen et al., 2014; Gueron-Sela et al.,
2015). Moreover, preterm-born infants whose mothers participated in a sensitivity training
program at the Neonatal Intensive Care Unit (NICU) showed improved cerebral white-matter
micro-structural development when they reached full-term age (Milgrom et al., 2010).
Unfortunately, dyads of mothers and their preterm-born infants may have less attuned in-
teractions than mothers and full-term infants, especially during the first 6 months of life (e.g.,
Harel-Gadassi et al., 2020; Vaccaro et al., 2021; but see Bilgin & Wolke, 2015). In particular, moth-
ers of preterm-born infants tend to be less sensitive, show less affectionate touch and be more
intrusive than mothers of full-term infants (e.g., Feldman & Eidelman, 2007; Korja et al., 2012;
Vaccaro et al., 2021). At the same time, preterm-born infants tend to show less positive mood and
are less engaged in interactions with their mothers than term-born infants (Harel et al., 2011).
Several explanations of these group differences have been offered. The early, unexpected, and
sometimes traumatic delivery of a preterm infant may lead to increased maternal self-blame and
concerns about an inability to protect the infant (Harel-Gadassi et al., 2020; Korja et al., 2012).
When this is coupled with a prolonged hospitalization in the NICU, which involves separation
from the newborn, maternal sensitivity may be compromised (Neri et al., 2017). Other explana-
tions focus on the infants. Preterm-born infants are abruptly and prematurely separated from
their optimal uterine environment to less optimal conditions; this might hamper the healthy
maturation process of the central nervous system, specifically the brain stem, the amygdala-
limbic system, and the prefrontal cortex (Feldman, 2006; Tamm et al., 2020). Consequently,
preterm-born infants may show more gaze aversion and less clear communicative intentions
(e.g., Feldman, 2006; Harel et al., 2011).
Our goal was to extend this literature. Specifically, we examined whether certain motor behav-
iors of infants born preterm may contribute to difficulties in the attunement of their interactions
with their mothers.
The first motor behavior we examined was infants’ spontaneous movements. Infants move spon-
taneously, i.e., without intention or a specific trigger, until the CA of 5 months. Spontaneous
movements appear over the entire body in variable sequences and complexity. Their richness
and complexity indicate the intactness of the neural system (e.g., Peyton et al., 2017). Thus, spon-
taneous movements are usually used to detect neurodevelopmental deficiencies, such as cerebral
palsy and minor neurological deficiencies (e.g., Einspieler et al., 2019). The highest predictive
value of infants’ spontaneous movements is between the CA of 3–5 months and is based on
the assessment of fidgety movements (FMs) and movement character (e.g., Bruggink et al., 2008;
Einspieler et al., 2019). Normal FMs are tiny and elegant movements, characterized by small
amplitudes, moderate speed, and variable accelerations of neck, trunk, and limbs in all directions
(Einspieler et al., 2004). Their appearance indicates a healthy nervous system. Typically, they
occur continuously or intermittently between 3 and 5 months CA (Ferrari et al., 2016). Abnormal
appearance of FMs manifests in larger amplitude, faster speed, and jerkiness; this type of FMs is
rare and indicates an increased risk for minor neurological deficiencies, such as developmental
coordination disorder (Bruggink et al., 2008, 2009). Finally, the absence of FMs indicates a high
risk for severe neurologic dysfunction, such as cerebral palsy (e.g., Einspieler et al., 2019).
LEV-ENACAB et al. | 415
The second motor behavior that may be associated with mother–infant attunement is infants’
achievement of motor milestones, which is typically assessed in routine pediatric checkups to
detect developmental delays and motor disorders (Di Rosa et al., 2016). It could be expected that
particularly during the first 6 months of life, slower achievement of motor milestones would be
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416 LEV-ENACAB et al.
associated with infants’ lower ability to respond to and initiate interactions with their moth-
ers. White-Traut et al. (2018) suggested faster achievement of head control, one of the main
achievements of motor development during the first months of life, is crucial for initiating and
preserving interactions with the mother. In addition, better stability of the trunk and the head in
supported sitting position enables infants to move their hands more easily toward midline and
toward their caregivers’ face and body. This, in turn, may facilitate infants’ responsiveness to and
involvement with their mothers (Iverson, 2010) and consequently facilitate maternal sensitivity.
Preterm-born infants generally present slower achievement of motor milestones than term-
born infants, especially during the first year of life (Di Rosa et al., 2016). Yet research on the
links between the achievement of motor milestones and the attunement of mother–infant in-
teractions is scant and inconsistent. Three studies found maternal sensitivity, non-intrusiveness,
and a related construct of mutual mother–infant responsiveness were associated with a faster
achievement of motor milestones of infants born preterm at the CA of 6 weeks (White-Traut
et al., 2018), 6 months (Feldman et al., 2002), and 12 months (Pridham et al., 2002). A fourth
study showed that infants with low birthweight, whose mothers touched them more frequently
at the CA of 3 months, achieved their motor milestones faster at 12 months CA (Weiss et al.,
2004). However, in a fifth study focusing on preterm infants at the CA of 9 months, the associa-
tion of maternal sensitivity and non-intrusiveness with faster motor milestone achievement was
documented only among preterm-born infants with extremely low birthweight and not among
preterm-born infants with low birthweight or full-term infants (Neri et al., 2017). Finally, in a
sixth study of preterm-born infants at the CA of 24 months, maternal sensitivity was associated
with slower achievement of motor milestones (Treyvaud et al., 2009). Hence, our second aim was
to reexamine the links between preterm-born infants’ achievement of motor milestones and the
attunement of their interactions with their mothers.
The third infants’ characteristic examined in this study was temperament. Temperament is con-
sidered a psychobiological characteristic that is evident in infants’ reactivity to stimuli in the
environment (Rothbart et al., 2000). It can be characterized along the following four dimensions:
Surgency refers to infants’ positive affectivity expressed via motor activity level, and smiling and
laughter (Gartstein & Rothbart, 2003). Negative affectivity reflects infants’ distress in response
to physical limitations (i.e., frustration) and sudden changes (i.e., fear; Gartstein & Rothbart,
2003). Soothability refers to the ability of infants to recover from distress in response to caregiv-
ers’ soothing efforts (Rothbart, 1986). The fourth dimension reflects self-regulation capacities
or the ability to self-modulate negative and positive affectivity. It involves skills that begin to
emerge at the age of 12 months. Yet one of its components, Duration of orientation, which taps
attention span to object or activity, is evident from birth (Rothbart, 1986).
It is important to consider temperament when studying infants’ motor behaviors because
during the young ages of 3–5 months, bodily movement is a central modality through which
temperament is expressed (Planalp et al., 2017). Surgency is reflected in the frequency and in-
tensity of gross movements and movements of the face when smiling and laughing (Gartstein
& Rothbart, 2003; Rothbart, 1986). Negative affectivity is manifested by extensive upper and
lower limb movements, squirming, and back arching (Egmose et al., 2019). Soothability is evi-
dent through changes in infants’ gross movements and movements of the face from movements
LEV-ENACAB et al. | 417
6 | T H E P RE SE N T ST U DY
mothers (Trevarthen & Aitken, 2001). Third, this age is optimal for evaluating spontaneous
movements because FMs are presumably at their best performance and continuity level during
this period (Ferrari et al., 2016).
We hypothesized that typical and continual spontaneous movements, more advanced motor
milestones, and less difficult temperament, in terms of higher surgency, lower negative affectiv-
ity, and higher soothability and duration of orientation would be associated with better attune-
ment of the mother–infant dyad. Put differently, we expected each of these infant characteristics
would be associated with higher maternal sensitivity, lower maternal intrusiveness, and higher
infants’ responsiveness to and involvement with the mother.
7 | M ET H OD
7.1 | Participants
The present study was conducted according to guidelines laid down in the Declaration of Helsinki,
with written informed consent obtained all parents before data collection. All procedures in this
study were approved by the Helsinki Ethics Committee at the Maccabi Health Care Services and
the Human Research Review Board of the University of Haifa, Israel (#201/2015). Sixty Israeli
mothers and their preterm-born infants participated in this study. Thirty-nine of these dyads
participated in our pilot study (Lev-Enacab et al., 2015). Dyads were recruited via flyers in NICUs
and pediatric clinics, and electronic flyers were published on social networks sites for mothers of
infants. Of the 80 mothers who responded to the flyers, eight refused to be video-recorded, and
11 postponed their approval; by the time they agreed, their infants were older than 22 weeks CA.
The remaining 61 mother–infant dyads participated in the study. Considering this was the first
study to examine the interplay between the aforementioned motor behaviors of infants born pre-
term and the attunement of their interactions with their mothers, we chose to focus on healthy
infants. Therefore, exclusion criteria were intra-uterine growth retardation, perinatal asphyxia,
genetic or metabolic diseases, hearing impairment, retinopathy of prematurity, major congenital
defects, oxygen treatment after release from the NICU, or any operation during or after hospi-
talization. One infant met one of the criteria. Data collected for this infant and her mother were
not included in analyses.
Thirty-seven (61.66%) mothers were Jewish native Israeli; 10 (16.67%) were Jewish Israeli im-
migrants from Eastern Europe, North America, or North Africa; 5 (8.33%) were Muslim–Arab
native Israeli; 4 (6.67%) were Christian–Arab native Israeli; 3 (5%) were Christian–non-Arab im-
migrants from Eastern Europe; 1 (1.67%) was Druze native Israeli. This distribution suggests
the sample was representative of the diverse Israeli society from which it was drawn (Israel
Central Bureau of Statistics, 2021). Mothers’ age range was 20–47 years (Mdn = 35, Interquartile
range = 31.25–38.00), and all except three were married. The educational level of the mothers
ranged from high school diploma (12 mothers, 20.00%) to a doctorate (1 mother, 1.67%). Forty-
eight (80.00%) had post-high school education.
Participating infants (35 males, 58.33%) were at the CA of 12 to 22 weeks (Mdn = 14,
Interquartile range = 13–16). Infant were born between 26 and 34 weeks of gestation (Mdn = 33,
Interquartile range = 30–34). Twenty (33.33%) were firstborns, and 19 (31.67%) were one of
twins. Only one twin from each pair was randomly selected for participation. Infants’ birth-
weight ranged from 715 to 2600 gr (M = 1763.92 gr, SD = 454.51). Thirty-five (58.33%) were
born in a cesarean labor. Seventeen (25.4%) did not need any medical interventions in the NIUC,
LEV-ENACAB et al. | 419
35 (52.2%) received mild interventions, such as phototherapy for neonatal jaundice, and nine
(13.4%) needed breathing support for more than 3 days or received caffeine therapy. Forty-one
(68.33%) mothers kangarooed their infant (i.e., held the infant “skin to skin”) in the NICU for at
least 4 days.
7.2 | Procedure
Data were collected during 2012–2014 by trained developmental physiotherapists. Home visits
were conducted for all participants except for three families who preferred to meet at the pediat-
ric clinic. The meeting was set at a time when the infant was likely to be awake and calm. If the
infant showed signs of distress during data collection, the assessment was stopped and resumed
only if the infant calmed down. The study procedures were as follows.
First, to assess infants’ spontaneous movements, we followed the protocol of the General
Movement Assessment according to Prechtl (Einspieler et al., 2004) and videotaped the in-
fants lying supine on a mattress, partially dressed, and without any stimulation for approx-
imately four minutes. During this time, mothers were asked to complete a temperament
questionnaire (The Infant Behavior Questionnaire; Rothbart, 1981) and a demographic ques-
tionnaire. One infant turned repeatedly to a side-lying position. Thus, the spontaneous move-
ments of this infant could not be assessed. Next, to assess the attunement of mother–infant
interactions, mothers were invited to join their infants on the mattress and play with them for
10 minutes as they usually did, but without any toys or a pacifier. This type of unstructured
“social play” is common in research of mother–infant and mother–child interactions (e.g.,
Miller & Harwood, 2002; Zreik et al., 2017). As we were interested in examining maternal
sensitivity in the modality of touch and holding, we asked the mothers to pick up the infant
from the mattress and put the infant down at least once during the interaction. The timing
of picking up, holding, and putting the infant down was the mothers’ choice. However, if the
mother did not pick up the infant or did not put the infant down on the mattress within nine
minutes, she was reminded to do so by the researcher. The mother–infant interactions were
videotaped. Finally, to assess motor milestones, infants were videotaped while positioned by
the researcher supine, prone, sitting, and standing in accordance with the administration
procedure of the Alberta Infant Motor Scale (AIMS; Piper et al., 1994). The assessment of
motor milestones of one infant was not completed, because the infant was distressed and did
not calm down.
7.3 | Assessments
This coding system was adapted by the first and second authors from the widely used Emotional
Availability Scales (EAS; Biringen et al., 2000; see a review in Biringen et al., 2014) (Lev-Enacab
& Sher-Censor, 2012). The second author is an expert coder of the EAS. In line with the EAS,
the MIA coding system examined maternal sensitivity and non-intrusiveness, as well as infants’
responsiveness and involvement. Because we were interested in examining maternal sensitiv-
ity separately in each modality, we expanded the maternal sensitivity scale from the EAS to
three subscales: sensitivity of touch and holding, sensitivity of vocalization, and sensitivity of eye
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420 LEV-ENACAB et al.
contact. The subscale of sensitivity of touch and holding was based also on the measurement of
maternal touch of preterm-born infants (Feldman, 1998; Feldman, Eidelman, et al., 2002).
Maternal sensitivity
As noted above, maternal sensitivity comprised three subscales.
Sensitivity in the modality of touch and holding was subscale consisted of sensitivity of touch
(i.e., kissing, patting, hugging, or using a deep touch the infant seemed to enjoy and while show-
ing positive affect toward the infant); sensitivity of picking up the infant from the mattress (i.e.,
gradually picking the infant up while keeping the infant's body, especially the head and hands,
gathered); sensitivity of holding the infant (i.e., in an attuned holding, the infant is held close to
the mother's body and the infant's head and neck are supported); sensitive speed of changing the
infant's position while held in the mother's arms (i.e., the mother changes the infant's position in
her arms gradually and is attentive to the infant's reactions); sensitivity of putting the infant down
on the mattress (i.e., the mother puts her infant down slowly and carefully while being attentive
to the infant and keeping the infant's body, especially head and neck, safe and gathered). Except
for sensitivity of touch, which was coded using a 7-point scale, the other aspects of maternal
sensitivity in the modality of touch and holding were rated using 6-point scales. The scores were
highly intercorrelated (.32 < r < .59, p's < .05, respectively). As we did not have specific hypoth-
eses for these modalities, we aggregated them based on their mean, after transforming them to
z-scores. Higher scores reflected higher sensitivity in the modality of touch and holding.
Sensitivity of vocalization was rated using a 6-point scale ranging from “1” non-sensitive vocal-
ization (i.e., using a hostile tone of voice or a very loud voice that seemed to startle the infant or
a verbal communication that was hostile to or mocked the infant) to “6” highly sensitive vocal-
ization (i.e., a pleasant vocalization and verbal communication that seemed to match the infant's
cues).
Sensitivity of eye contact was coded on a 6-point scale ranging from “1” low sensitivity (i.e.,
mothers who avoided eye contact) to “6” high sensitivity (i.e., mothers who frequently looked at
their infants, in a manner attuned to the infants, thereby creating a synchronized eye contact).
The intercorrelations of the scores of mothers’ sensitivity of touch and holding, vocalization,
and eye contact were high and ranged from.57 to.79, p's < .05. Hence, we formed a maternal sen-
sitivity aggregated score by averaging their z-scores.
Maternal Non-Intrusiveness
Mothers were rated on a 6-point non-intrusiveness scale, reflecting their respect of the infant's
autonomy. High scores represented lack of interference in and interruptions of the infant's move-
ments and positions. Lower scores indicated that mothers were overstimulating, changing in-
fants’ positions frequently and abruptly, interfering with their activity, or overprotecting them.
Infants’ responsiveness
This 6-point scale reflected infants’ response to their mothers’ interactive suggestions. A score
of “1” represented avoidance or reluctance to engage with the mother, and a score of “6” repre-
sented responses to maternal suggestions with a positive affect.
Infants’ involvement
This 6-point scale indicated infants’ initiations of interaction with their mother by, for example,
making eye contact. A score of “1” represented lack of initiations and “6” represented frequent
initiations.
LEV-ENACAB et al. | 421
As the correlation between infants’ responsiveness and involvement was high (r = .90,
p < .01), and as we did not have specific hypotheses for either scale, we combined their mean
scores to one scale, infants’ attunement.
The fifth author, who was blind to other information regarding the families, was trained by
the first author and coded the dyadic interactions. To establish reliability, 15 (25%) dyads were
also coded by the first author. Both coders were developmental physiotherapists with an MA in
child development. Inter-rater agreement of the MIA scales was good and ranged from ICC = .83
(sensitivity of holding the infant) to ICC = .99 (sensitivity of vocalization). Average ICC across
scales was .93. Disagreements were resolved through discussion, until consensus was reached.
For information on the reliability and validity of the MIA scales obtained in our pilot study, see
Lev-Enacab et al. (2015).
The GMA is widely used to assess infants’ spontaneous movements and is considered the most ac-
curate for early diagnosis of neurodevelopmental disorders (e.g., Bruggink et al., 2009; Einspieler
et al., 2019, 2004; Snider et al., 2008). We used the GMA to code the following aspects of infants’
spontaneous movements.
Movement character
Movement character reflects the variability, complexity, and sequence of movements of the
limbs, neck, and trunk. Smooth and fluent, variable, and complex movements were scored as
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422 LEV-ENACAB et al.
“2” (typical). We assigned a score of "1" (atypical) when the infant showed monotonous, jerky,
or stiff movements, movements with large or small amplitude, or movements with reduced com-
plexity. A cramped synchronized movement (e.g., limbs and trunk muscles contracting almost
simultaneously and relaxing almost simultaneously) was scored as “0” (abnormal; Einspieler
et al., 2019). None of the participating infants showed abnormal movement character. As the
FMs temporal organization and movement character were closely associated (Kendall's T = .51,
p < .01) and to reduce the number of variables, we computed the mean of the two scores. We
labeled the new construct infants’ spontaneous movements. Scores ranged from “0” to “2”, with
higher scores reflecting typical and continual spontaneous movements.
Video recordings of infants’ spontaneous movements were assessed by the first author, a de-
velopmental physiotherapist with an MA in Child Development, who was certified for coding
the GMA. To establish inter-rater reliability, the third author, a physiologist and an expert and
licensed tutor for the GMA, who was blind to all other information on the participants, also
coded 30 video recordings (50.00%). These included the 15 dyads for whom, as described above,
the first author coded the MIA scores. Inter-rater agreement was good (KappaFMs continuity = .69;
KappaMovement Character = 1.00). Agreement was comparable to or exceeded the inter-rater agree-
ment reported in prior research (e.g., Einspieler et al., 2019). Disagreements were resolved
through discussion until consensus was reached.
The AIMS is a widely used motor development assessment. It is commonly used in clinics and
research settings to assess motor delays in term-born and preterm-born infants (e.g., Knorr et al.,
2017; Piper et al., 1994). The AIMS examines the rate of infants’ achievement of motor milestones
from birth to 18 months, as observed in four positions: supine, prone, sitting, and standing. The
observer minimally intervenes when needed by positioning the infant and/or by playing with
the infant to encourage the infant to exhibit the most advanced motor milestones. To calculate
the AIMS score, the number of fully performed milestones is calculated for each position sepa-
rately and summed to a total raw score. Next, the total raw score is converted to a percentile
age-dependent norm scale (Darrah et al., 1998). A cutoff point of less than 10th percentile has
70% sensitivity to later motor deficiencies (Darrah et al., 1998). We converted the percentile raw
scales to a 6-point scale, ranging from “1” (below 5th percentile) to “6” (above 75th percentile).
The assessments were videotaped and rated by the fourth author, a developmental physiother-
apist, who is well trained and qualified to use the AIMS coding system. She was blind to all other
information on the participants. The first author also coded 15 of the cases (25%) for inter-rater
reliability, which was excellent (ICC = .94), similar to previous reports (ICC = .99; Piper et al.,
1992). These 15 cases were the same as the ones for whom the first author coded the MIA scores.
approaching at once when introduced to a dog or a cat and soothing in responses to a security
object). The third was an open-ended question regarding “other soothing techniques” which
mothers tended to use.
The remaining 91 items were grouped to four dimensions (Rothbart, 1986). Surgency in-
cluded 32 items reflecting level of motor activity, which indicated the frequency and intensity of
infants’ gross movements during daily activities (e.g., “During feeding, how often did the baby
squirm or kick?”), and smiling and laugher under safe conditions (e.g., “When put into bath
water, how often did the baby smile?”). Negative affectivity included 39 items reflecting infants’
distress to limitation, namely, fussing and crying when waiting for food or put in a confining
place or position (e.g., “How often during the last week did the baby protest when being put in
a confining place [infant seat, play pen, car seat, etc.]?”); and fear reactions, namely showing
distress in response to sudden changes and latency of movement toward a new person or object
(e.g., “How often during the last week did the baby cry or show distress at a loud sound [blender,
vacuum cleaner, etc.]?”). Soothability included nine items tapping infants’ reduced fussing and
crying in response to mothers’ soothing efforts (e.g., “Have you tried the technique of rocking in
the past two weeks? If so, how often did this method soothe the baby?”). Duration of orientation
was consisted of 11 items capturing infants’ attention span when looking at or interacting with a
single object or activity (e.g., “How often did the baby repeat the same movement with an object
for 2 min or longer [e.g., kicking or hitting a mobile]?”). After reveres coding of relevant items,
internal reliability was calculated using Cronbach's α; it was .89 for surgency, .95 for negative
affectivity, .78 for soothability, and .87 for duration of orientation.
Mothers were invited to complete a demographic questionnaire on their age, education level,
family status, number of children, birth order, ethno-cultural origin, and infant gender. In addi-
tion, they were asked to report the infants’ birth week of gestation, birth date, birthweight, length
of stay in the NICU, medical interventions the infant received and the use of kangaroo care in
the NICU.
8 | R E S U LTS
Descriptive statistics are provided in Table 1. The distribution of all variables was sufficiently
normal to render parametric statistics valid (Afifi et al., 2007). The following background vari-
ables were associated with the study variables: lower birthweight was correlated with slower
achievement of motor milestones (r = .28, p = .032) and older maternal age and birth order
were related to mothers’ reports of lower levels of infants’ surgency (r = −.30 p = .022; r = −.33,
p = .012 respectively). Thus, birthweight, mother age, and birth order were considered in further
analyses.
The study hypothesis was first examined using bivariate correlations between infants’ charac-
teristics (i.e., spontaneous movements, achievement of motor milestones, temperament dimen-
sions) and the mother–infant attunement. As shown in Table 2, infants’ typical and continual
spontaneous movements were associated with higher maternal sensitivity and non-intrusiveness,
as well as higher infant attunement. Faster achievement of motor milestones was significantly
associated with higher maternal non-intrusiveness but not with maternal sensitivity or infant
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424 LEV-ENACAB et al.
1 2 3 4 5 6 7 8 9
1. Maternal sensitivity – .74** .71** .36* .07 −.22 −.07 −.27* −.25
2. Maternal non-intrusiveness – .52** .46** .30* −.23 −.09 −.17 −.20
3. Infant attunement – .36** .09 −.10 −.07 −.03 −.08
4. Infants’ spontaneous – .36** .03 .16 .12 −.06
movementsa
5. Infants’ achievement of motor – −.03 −.07 −.01 −.15
milestones
6. Infants’ surgency – .−.05 .32* .52*
7. Infants’ negative affectivity – −.06 −.07
8. Infants’ soothability – .22
9. Infants’ duration of orientation –
a
Associations involving spontaneous movements were evaluated using the Spearman tests.
*p < .05; **p < .01.
attunement. Lower soothability was significantly associated with higher maternal sensitivity but
not with maternal non-intrusiveness or infant attunement. Infants’ surgency, negative affectivity,
and duration of ordination were not related to mother–infant attunement.
In the next step, we conducted regression analyses. Maternal sensitivity and maternal non-
intrusiveness were the dependent variables in the regression models. The results of correlation
analyses informed the selection of variables for each model. Among background variables, only
birthweight was associated with a study variable that was significantly correlated with mother–
infant attunement, namely infants’ achievement of motor milestones, and hence it was the
LEV-ENACAB et al. | 425
only background variable included in the regression analyses. The first block of the regression
model of maternal sensitivity included infants’ soothability; this was followed by infants’ sponta-
neous movements in the second block. The first block of the regression model of maternal non-
intrusiveness included infants’ birthweight. The second block included infants’ achievement of
motor milestones; this was followed by spontaneous movements in the third block. We included
soothability or the achievement of motor milestones and spontaneous movements in separate
blocks because we wanted to document the unique contribution of each of these variables to the
explained variance of the attunement of mother–infant interaction. Spontaneous movements
were entered in the final block because we wanted to examine its added value in research of
mother–infant interaction, which to the best of our knowledge was not examined thus far.
As Table 3 shows, both soothability and infants’ spontaneous movements contributed sig-
nificantly to the explained variance in maternal sensitivity. Lower soothability and typical
and continual spontaneous movements were associated with higher maternal sensitivity. As
also shown in Table 3, faster achievement of motor milestones was significantly associated
with higher levels of maternal non-intrusiveness after controlling for infant birthweight.
Yet the effect became non-significant when we included spontaneous movements in the re-
gression model. Only the spontaneous movements contributed significantly to the explained
variance of maternal non-intrusiveness in the final regression model. More specifically, in-
fants’ typical and continual spontaneous movements were associated with higher maternal
non-intrusiveness.
9 | DI S C USSION
Our goal was to identify characteristics of preterm-born infants that are associated with the
attunement of mother–infant interactions, looking specifically at motor behaviors. We found
infants’ spontaneous movement was the only characteristic consistently associated with attune-
ment. As hypothesized, typical and continual spontaneous movements were associated with
|
426 LEV-ENACAB et al.
mothers’ attunement in terms of higher maternal sensitivity and non-intrusiveness and with
infants’ attunement in terms of higher responsiveness and involvement.
Previous work has found infants’ cuteness facilitates parental caretaking and fosters increased
attention and positive affect toward the infant (Glocker et al., 2009; Golle et al., 2015; Kringelbach
et al., 2016). Thus, the elegancy and cuteness of infants’ smooth and fluent gross movements that
accompany the continual expression of FMs (de Raeymaecker, 2006; Einspieler et al., 2016, 2019)
may facilitate mothers’ positive affect and responsiveness. Infants with repetitive and/or stiff
movements with low/intermittent continuity of FMs may look less cute in their movements, and
this may lead to less frequent expressions of positive affect by their mothers (Golle et al., 2015).
At the same time, infants’ smooth and fluent spontaneous movements may enable them to
initiate and maintain positive engagement in the interaction. Repetitive, jerky, and stiff move-
ments may hamper infants’ ability to bring their arms and legs to and maintain them at the
midline or at the direction of their mother's face (Fjørtoft et al., 2016), thus limiting their ability
to initiate and maintain interactions (Egmose et al., 2019). Mothers may unintentionally respond
to these difficulties in less sensitive and more intrusive ways. For example, mothers may unin-
tentionally “chase” their infants and intrusively move the infants’ body and face toward them to
maintain longer eye-to-eye contact and turn-taking. Infants’ jerky and stiff movements may also
lead mothers to hold the infants too tightly and change their position abruptly and firmly when
picking up, holding, and putting the infants down.
Another interpretation of the association between infants’ spontaneous movements and
mother–infant attunement is that infants’ more typical and continual spontaneous movements
could be a proxy for a less medically involved course of recovery from preterm birth and/or a
less complicated medical situations, which led to a preterm birth, with these infants being more
capable of engaging in the interaction. In line with the study of Fjørtoft et al. (2016), our data
did not reveal significant associations between infants’ gestational age, medical condition or
interventions in the NICU and their spontaneous movements or mother-–infant attunement.
Nevertheless, future studies may benefit from assessing more thoroughly various prenatal and
postnatal medical risks.
The results of this research replicated those of our pilot study's smaller sample (Lev-Enacab
et al., 2015). We have extended this earlier work by documenting that spontaneous movements
are associated not only with maternal sensitivity and infant attunement but also with mater-
nal non-intrusiveness and by showing that the links between the spontaneous movements and
mother–infant attunement hold when controlling for two additional characteristics of the in-
fants, achievement of motor milestones and temperament. To the best of our knowledge, these
are the only two studies to examine links between spontaneous movement and early mother–
infant interaction. Additional studies are needed to replicate the results.
The current study indicated that faster achievement of motor milestones was correlated only
with maternal non-intrusiveness, not with maternal sensitivity or infant attunement. Moreover,
the link between the achievement of motor milestones and maternal non-intrusiveness became
non-significant when taking into account infants’ spontaneous movements. Our research joins
the few studies on this issue. Previous work has reported inconsistent results (Feldman, Eidelman,
et al., 2002; Pridham et al., 2002; Weiss et al., 2004; White-Traut et al., 2018; versus Neri et al.,
2017; Treyvaud et al., 2009). Notably, only one of these studies involved infants younger than
6 months (White-Traut et al., 2018). This study documented a positive effect of an early interven-
tion program for mothers of preterm infants on the motor development of the infants at the CA
of 6 weeks. All other studies included older infants. Younger infants have fewer motor abilities;
hence, the differences between fast and slow achievement of motor milestones (i.e., infants who
LEV-ENACAB et al. | 427
are classified at the 75th percentile or above and those classified at or below the 5th percentile;
Piper et al., 1994) are smaller. This may hinder the ability to detect significant associations with
infant-mother interactions. Future studies may benefit from a wider age range of infants born
preterm to further understand whether the achievement of motor milestones is associated with
the attunement of mother–infant interactions.
Our hypothesis of an association between infants’ difficult temperament and lower attune-
ment of interactions was not supported. Unexpectedly, only one aspect of infants’ tempera-
ment was associated with only one aspect of mother–infant interactions, and the direction of
the association was contrary to our hypothesis: Higher soothability was associated with lower
maternal sensitivity. This finding suggests that mothers who reported their infants were more
adaptive to their soothing techniques tended to respond to their infants’ signals in a less attuned
manner. A possible explanation of this finding is related to the fact that infants’ soothability
was reported by the mothers. Maternal sensitivity involves accurate interpretation of infants’
emotional states and emotional needs (Ainsworth, 1969). It could be that less sensitive mothers
tended unintentionally to perceive their infants’ soothability less accurately, and viewed them
as needing less or briefer soothing to recover from distress (Benoit et al., 1997).
Prior research with older infants born preterm did not find significant links between tem-
perament and the quality of mother–infant interactions (e.g., Poehlmann et al., 2012; Vaccaro
et al., 2021). We are aware of one study of 3-month-old preterm-born infants that examined this
link. Unlike our study, this study found infants’ duration of orientation and self-modulation of
emotional arousal (the latter measure is not included in the mothers’ self-reports we used) were
associated with higher mother–infant synchronization, rated using a microanalytic coding sys-
tem (Feldman, 2006). As our study and this former research used different measures of infant
temperament and mother–infant interactions, more research is needed to shed light on whether
infant temperament is related to preterm-born infants’ and mothers’ behaviors during early in-
teractions. Future studies may also benefit from recruiting larger samples to better examine the
potential moderating role of temperament in the links between infants’ motor behaviors and
mother–infant attunement (Ghera et al., 2006).
Several limitations of the study suggest fruitful directions for future research. First, data were
collected concurrently, thus precluding the interpretation of causal effects. Spontaneous move-
ment, the achievement of motor milestones, and soothability may shape the behavior of the infant
and consequently the behavior of the mother during shared interactions. Nevertheless, mother–
infant interactions may also influence infants’ motor behaviors, and color maternal reports of
infants’ soothability. A recent pilot study of an early intervention for preterm-born infants with
abnormal movement character, in which the medical staff and parents practiced typical and con-
tinual sequences of movement character with the infants, found this intervention improved in-
fants’ spontaneous movements (Soloveichick et al., 2020). Furthermore, the infants in this study
showed normal motor and cognitive development at the ages of 2 and 4 years (Soloveichick et al.,
2020). Such intervention studies, as well as longitudinal studies, are needed to enrich our un-
derstanding of the bi-directional associations between motor behaviors of infants born preterm
and their early interactions with their parents. The second limitation is the sample selection; we
included only low-risk families (i.e., the majority of mothers were married and had a high level
of education) and low-risk preterm-born infants (none had cramped synchronized movements,
and all were healthy preterm-born infants). More research is required before we can generalize
our findings to high-risk dyads.
Despite these limitations, our research suggests the evaluation of spontaneous movements of
preterm-born infants, typically used to detect early neurological deficiencies (Einspieler et al.,
|
428 LEV-ENACAB et al.
2019), should be included in research on early interactions between preterm-born infants and
their mothers. Our study also suggests that early intervention and prevention programs for par-
ents of preterm-born infants should attempt to raise the awareness of parents regarding infants’
spontaneous movements and soothability and their possible associations with the attunement of
parent–infant interactions.
ACKNOWLEDGEMENTS
This research was supported by the Israeli Physiotherapy Society, Maccabi Health Care Service
and the Herta and Paul Amir Faculty of Social Sciences, University of Haifa, Israel. We would
like to thank the families who participated in this research, and Einav Manor from the NICU in
Rambam Hospital, Haifa, Israel, for her help in the recruitment of families.
CONFLICT OF I NTEREST
The third author, Professor Einspieler Christa is a licensed tutor of the General Movement
Assessment (GMA) according to Prechtl.
ORCID
Efrat Sher-Censor https://orcid.org/0000-0003-2961-3129
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