Review Article

Parent-Infant Interaction during the First Year of Life in Infants at High Risk for Cerebral Palsy: A Systematic Review of the Literature

Table 1

Characteristics of the included studies.

StudyAt high-risk sampleControl sampleExclusion criteriaTiming of assessmentMethodMain resultsStudy quality

Greene et al. [39]16 PT, with RDS
(S-PT)
16 FT, with birth asphyxia
(S-FT)
14 PT, healthy
(H-PT)
16 FT, healthy
(H-FT)
Not definedAt 3 months
(CA)
(i) Free play interaction
(ii) Video recording: 15 min
(iii) At the laboratory
(iv) Checklist by Lewis [40]
(i) Infant—look/gaze at mother:
H-PT, H-FT > S-PT, S-FT
(ii) Mother–vocal responsivity: H-PT, S-PT > H-FT, S-FT
(iii) Mother–proximal and kinesthetic stimulation: S-FT > S-PT, H-FT, H-PT
(iv) Mother—affective and distal stimulation: S-FT < S-PT, H-FT, H-PT
Other measures: S-FT, S-PT lower scores in orientation cluster at NBAS
Good

Lasky et al. [41]40 PT, BW <1500 g and/or requiring mechanical ventilation
(PT)
25 FT, healthy
(H-FT)
Not definedAt 12 months
(CA)
(i) Free interaction in 5 different situations: waiting, physical exam with a nurse present, physical exam with the nurse absent, the nurse return, and blood drawing
(ii) Live observation: 5, 2, 2, 2, and 4 min, respectively
(iii) At the hospital
(iv) Checklist by Lasky et al. [41]
(i) Mother—restrain infant, positioning near infant, looking at the infant, not smiling at infant during blood draw: H-FT > PT
Other measures: Bayley Mental Developmental Index (MDI) and Psychomotor Developmental Index (PDI): PT < H-FT
Good

Minde et al. [42]20 PT, BW <1500 g
(PT)
20 FT, healthy
(H-FT)
No physical malformationAt 1, 2, and 3 months
(CA)
-Visit 1 and 2: routine feeding, visit 3: face-to-face play sequence.
-Live observation, visits 1-2: duration not reported, visit 3: 10 min
-At home
-Scoring of infant and maternal behaviors (as in Minde et al. [43])
(i) Feeding 4 weeks:
Infant—alert/focused: H-FT>PT
Mother—look en face: PT>H-FT
Mother—vocalize to others: PT>H-FT
Mother—touch: PT<H-FT
Mother—smile: PT<H-FT
(ii) Feeding 8 weeks:
Infant—leg movements: H-FT>PT
Mother—vocalize to others: PT>H-FT
Mother—vocalize to baby: PT>H-FT
Mother—touch: PT<H-FT
Mother—smile: PT<H-FT
(iii) Play 12 weeks:
Infant—head/mouth movements: PT>H-FT
Mother—look: PT>H-FT
Mother—vocalize to baby: PT>H-FT
Mother—smile: PT<H-FT
Other measure: “Sicker infants” defined according to a morbidity scale by Minde et al. [44] display more behavioral disorganization during feeding, cry more, and have their eyes open.
Good

Landry et al. [45]20 high-risk (HR) PT with IVH III-IV, RDS, or BPD
(HR-PT)
20 low-risk (LR) PT with transient to moderate RDS and/or IVH I-II
(LR-PT)
20 FT: healthy full term
(H-FT)
Not defined12 months
(CA)
-Free play interaction
-Video recording—10 min
-At the laboratory
-Coding of mothers’ attention-directing and infants’ exploratory strategies [45]
-Mother—attention-directing behaviors: HR-PT>LR-PT, H-FT;
-Mother—questions: H-FT>LR-PT=HR-PT
Other measures: mothers of HR-PT used questions more often with infants with higher MDI, while they use attention-directing gestures with infants with lower MDI
Good

Farel et al. [46]37 High-risk (HR) infants with intracranial hemorrhage and/or perinatal asphyxia and/or seizures and/or meningitis and/or
(HR)
37 healthy (H) infants matched for age, sex, and raceNot definedAt 8 months (CA)-Interactions during a feeding episode, a session in which the mother is asked to teach the child an age-appropriate task and a free play session.
-Live observation: 120 min in total
-At home
-NCAFS, NCATS, and HOME scale (including an interview to the mother) [47, 48]
(i) Dyads—scores at NCAFS and NCATS: HR<H
Other measures: a strong association between NCAFS and risk status was reported
Poor

Landry et al. [49]11 PT with IVH III or IV
(HR-PT)
16 PT with RDS or IVH I and II
(LR-PT)
12 FT, healthy
(H-FT)
Other medical complicationsAt 12 months
(CA)
-Toy-centered play interaction
-Video recording: 10 min
-At the laboratory
-Coding of mother’s attention-directing and infant’s exploratory strategies [45]
-Infant—exploratory play in response to mother’s structured strategy: LR-PT>H-FT
-Infant—exploratory play: HR-PT<H-FT, and LR-PT
-Infant—exploratory play in response to unstructured versus structured strategies: H-FT>LR-PT, HR-PT
-Infant—exploratory play in response to structured versus unstructured strategies: LR-PT>H-FT, HR-PT
Fair

Smith et al. [50]89 PT with BPD, IVH III or IV, and/or PVL (HR-PT)123 PT with IVH I or II, transient RDS
(LR-PT)
128 FT: healthy
(H-FT)
Sensory impairments, meningitis, encephalitis, congenital abnormality of the brainAt 6 and 12 months (CA)-Toy play session and naturalistic observation of daily activity
-Live observation—10 min and 60 min
-At home
-Mixed rating scale and microanalytic coding system [45, 50]
(i) Daily activities and toy play at 6 and 12 months:
Mother—interactive behaviors:
HR-PT=LR-PT-H-FT
Other measures:
6 months
(i) MDI, daily living, receptive language:
FT, LR-PT>HR-PT
(ii) Expressive language:
HR-PT<H-FT
(iii) Positive correlation between mother attention maintaining behavior and infant mental age and receptive language score (during daily activity and toy play): HR-PT, LR-PT>H-FT
(iv) Positive correlation between mother attention maintaining behavior and infant expressive language score (during daily living activity): HR-PT, LR-PT>H-FT
(v) Positive correlation between mother—attention maintaining behavior and infant expressive language score (during toy play):HR-PT>LR-PT, H-FT
Fair

Schermann-Eizirik et al. [51]67 PT, was required IC
(VPTIC)
75 PT, was required IC
(PTIC)
66 FT, required IC
(FTIC)
IC, intensive care for CPAP or parenteral nutrition o severe asphyxia
70 FT, healthy
(H-FT)
Chromosoml abnormalities and severe cerebral malformations.At 2, 4, and 6 months
(CA)
-Interaction during undressing of the infant and face-to-face situation
-Video recording—variable time, 3 min
-At the laboratory
-Mother-infant interaction coding [52]
2,4,6 months:
-Mother—interactive behaviors: VPTIC, PTIC=H-FT
-Infant—interactive behaviors:
VPTIC, PTIC=H-FT
-Dyad—positive interaction:
VPTIC, PTIC=H-FT
2 months:
-Mother—interactive behaviors:
FTIC=FT
-Infant—interactive behaviors:
FTIC=FT
4 months:
Mother—sensitivity/involvement:
FTIC<FT
Infant—interactive behaviors:
FTIC<FT
Dyad—positive interaction:
FTIC<FT
(iv) 6 months:
Mother—sensitivity/involvement:
FTIC<FT
Infant—interactive behaviors: FTIC=FT
Good

Davis et al. (2003) [53]50 PT, BW < 1500 g, with neurobiological risk (defined by NBRS)
(HR-PT)
Normative dataNo congenital anomaliesWithin the 6th month-Interaction during feeding
-Video recording—20 min
-At home
-NCAFS [47]
(i) Total feeding score:
HR-PT<normative data
(ii) Mother—interactive behaviors:
HR-PT=normative data
(iii) Infant—responsivity to caregiver:
HR-PT<normative data
Other measures: mothers who coped better had more responsive children at three months after discharge, according to the Coping Health Inventory for Parents [54]
Fair

Muller-nix et al. [55]28PT, high-risk (HR) PT, defined by PERI [56]
(HR-PT)
19 low-risk (LR) PT, PT, defined by PERI
(LR-PT)
25 FT, healthy
(H-FT)
Infant malformation, chromosomic abnormalities, foethopatyAt 6 months (CA)-Mother-child toy-play interaction
-Video recording: 10 minutes
-Context not specified
-CARE index [57]
(i) Mother—sensitivity:
HR<LR<FT
(ii) Infant—interactive behaviors:
HR-PT=LR-PT-H-FT
Other measures:
Mother—posttraumatic stress symptoms:
HR-PT>FT
More stressed mothers were less sensitive and more controlling in dyadic play
Fair

Schmücker et al. (2005) [58]79 PT, BW < 1500 g, and/or with IVH, PVL, SGA or required more than 28 days on mechanical ventilation
(HR-PT)
35 FT, healthy (H-FT)Not definedAt 3 months (CA)-Interaction during diaper change and free play
-Video recording—10 minutes
-At the laboratory
-Microanalytic coding system to rate early mother–child interaction [59]
-Infant-vocalize:
HR-PT>H-FT
-Infant-vocally responsive:
HR-PT>H-FT
-Infant—facially responsive:
HR-PT<H-FT
Mother—facially responsive:
HR-PT<H-FT
Other measures:
The higher the neurobiological risk of the infant, the more mothers were judged to lack sensitivity
Fair

Feldman (2006) [60]17 PT, BW: < 1000 g, GA < 30 ws
(HR-PT)
25 PT BW= 1700-1850
g, GA = 34-35 ws
(LR-PT)
29 FT: GA >2500 g
> 36 ws, (H-FT)
IVH III and IV, asphyxia, metabolic and genetic diseases.At 3 months (CA)-Face-to-face interaction
-Video recording: 5 min
-At home
-Scoring with Monadic Phase Manual [61]
-Mother-infant synchrony:
H-FT>HR-PT, LR-PT
HR-PT=LR-PT
-Mother-infant degree of synchrony (coherence):
FT>LR-PT>HR-PT
-Infant—negative emotionality:
HR-PT, LR-PT>H-FT
Other measures: Biological rhythm analysis revealed that sleep–wake cyclicity, vagal tone, orientation, and arousal modulation are each uniquely predictive of mother–infant synchrony at 3 months
Good

Feldman and
Eidelman [62]
18 PT, SGA, BW: <1000 g
(SGA< 1000)
28 PT, AGA, BW: <1000 g
(AGA< 1000)
22 PT, SGA, BW: >1000 g
()
52 PT, AGA, BW: >1000 g
()
IVH IV, asphyxia, metabolic or genetic or syndromic disease, SNC infectionsAt 3 months (CA)-Mother-infant interaction
-Video recording: 10 min
-At home
-CIB [63]
Mother-intrusiveness:
(SGA<1000)>(SGA>1000)>(AGA<1000), (AGA>1000)
Infant—negative engagement:

Other measures:
At 12 months, showed poorer cognitive development at MDI. scored significantly lower on orientation and motor maturity compared with other groups
Good

Feldman [64]34 PT, BW < 1500 g;
(HR-PT)
21 PT, IUGR, <1500 g
(HR-PT)
38 FT: healthy
(H-FT)
Maternal and/or paternal depression and anxietyAt 4 months
(CA)
-Interaction mother-infant father-infant, triadic interaction
-Video recording: 5 min each
-At home
-Coding Interactive Behavior (CIB) Manual [63]
-Mother—intrusiveness: HR-PT>H-FT
-Mother—sensitivity: HR-PT<H-FT
-Infant—negative emotionality: HR-PT>H-FT
-Dyad—reciprocity: HR-PT<H-FT
Other measures:
(i) Family cohesion: HR-PT<FT
-Family rigidity: HR-PT>FT
Mother of IUGR infants showed the highest intrusiveness scores and IUGR infants showed the highest negative emotionality. Family also showed the highest rigidity
Good

Korja et al. [65]30 PT, BW
<1500 g, GA: <32 WS
(PT)
36 FT: healthy
(H-FT)
Major congenital
anomalies
At 6 and 12 months (CA)-Free play mother-infant interaction (toy optional)
-Video recording: 5 min
-At the laboratory
-PC-ERA [66]
-6 months:
Infant—interactive behaviors: PT=H-FT
Mother—interactive behaviors: PT=H-FT
-12 months:
Infant—quality of play and attention: PT<H-FT
Infant-sober and withdrawn: PT<H-FT
Mother—interactive behaviors: PT=H-FT
Other measures: duration of holding at 5 months (CA) was positively associated with the good quality of mother–infant interaction at 6 and 12 months in PTPTs cried (combined fussing and crying) more often and were held more than H-FT
Good

Agostini et al. [67]29 PT, BW: <1000 g
(HR-PT)
40 PT, BW: <1500 g
(PT)
80 FT healthy
(H-FT)
Infant chromosomal abnormalities, CP, malformations and foetopathyAt 3 months
(CA)
-Face-to-face interaction
-Video recording: 5 min
-At the laboratory
-Global rating scale (GRS) [68]
-Mother—sensitivity: HR-PT=PT=H-FT
-Mother—intrusiveness: HR-PT>H-FT
-Mother—remoteness: PT, HR-PT<H-FT
-Infant—interactive behaviors: HR-PT=PT=H-FT
Other measures:
In H-FT mothers, higher degree of remoteness was associated to the presence of depressive symptoms
Good

Neri et al. [69]32 PT, BW: <1000 g
(HR-PT)
45 PT, BW <1500 g
(PT)
20 FT, healthy
(H-FT)
Infant chromosomal abnormalities, cerebral palsy, malformations and foetopathyAt 3 months
(CA)
-Face-to-face interaction
-Video recording: 5 min
-At the laboratory
-Global rating scale (GRS) [68]
-Mother—sensitivity: PT>H-FT
-Mother—intrusiveness: HR-PT>H-FT
-Mother—remoteness: HR-PT<H-FT
-Infant—communicative dimension: PT>FT
Other measures:
Mother—signs of depression:
HR-PT, PT>H-FT
Good

Sansavini et al., 2015 [70]20 PT: ws
(HR-PT)
20 FT: >37 ws
(H-FT)
Major cerebral damage,
PVL, IVH > II grade, hydrocephalus
At 12 months
(CA)
-Mother-child toy-play interaction
-Video recording: 10 minutes
-At the laboratory
-R-RCS for dyadic coregulation and Lunkenheimer’s coding system for coding affective intensity [71, 72]
-Dyad—frequency of symmetric coregulation patterns: HR-PT<H-FT
-Dyad—frequency of unilateral coregulation patterns: HR-PT>H-FT
-Infant—emotional Involvement: HR-PT<H-FT
-Mother—frequency of high positive affective intensity: HR-PT<H-FT
Infant—frequency of neutral affective intensity: HR-PT>H-FT
Infant—frequency of high positive affective intensity: HR-PT<H-FT
Infant—frequency of low positive affective intensity: HR-PT>H-FT
Infant—duration of neutral affective intensity: HR-PT>H-FT
Infant—duration of high positive affective intensity: HR-PT<H-FT
Infant—duration of low positive affective intensity: HR-PT<H-FT
Infant—duration of neutral affective intensity: HR-PT>H-FT
Infant—duration of low negative affective intensity: HR-PT>H-FT
Fair

AGA = appropriate for gestational age; BPD = bronchopulmonary dysplasia; BW = birth weight; CA = corrected age; CIB = coding interactive behavior; FT = full-term infant; GA = gestational age; H-FT = healthy full term; H-PT = healthy preterm; HOME = Home Observation Measurement of the Environment; HR-PT = high-risk preterm; IUGR = intrauterine growth retardation = IVH: intraventricular hemorrhage; LR-PT = low-risk preterm; MDI = Bayley Mental Developmental Index; NBAS = Neonatal Behavioral Assessment Scale; NBRS = Neurobiological Risk Score; NCAFS = Nursing Child Assessment Feeding Scale; NCATS = Nursing Child Assessment Teaching Scale; PC-ERA = Parent-Child Early Relational Assessment; PDI = Bayley Psychomotor Developmental Index; PT = preterm infant; PTIC = preterm who required intensive care; PVL = periventricular leukomalacia; RDS = respiratory distress syndrome; S-FT = sick full term; S-PT = sick preterm; SGA = small for gestational age; VPTIC = very preterm who required intensive care. Assessed through National Heart, Lung, and Blood Institute (NHLBI) Quality Assessment Tool for Case-Control Studies [38].