Abstract
Background:
Parent-infant interaction is poorly understood among high-risk dyads in NICU settings. No parent-infant interaction measures are specifically designed for preterm infants within the NICU nor account for the education NICU parents receive to tailor their interactions based on the infant's cues.
Aim:
To improve our understanding of a measure of parent-infant interaction in the NICU, we investigated relationships between parent-infant interaction scores on the Nursing Child Assessment Feeding Scale (NCAFS) and 1) socio-demographic and medical factors, 2) parent mental health and confidence, and 3) enhanced parental education (delivered as part of the Supporting and Enhancing NICU Sensory Experiences program) on tailoring interactions based on the infant's cues.
Method:
Twenty-six preterm infants (born ≤32 weeks) had a video recorded oral feeding conducted by a parent in the NICU when the infant was 34–48 weeks postmenstrual age. A certified evaluator scored parent-infant interaction from the videos using the NCAFS.
Results:
Seventeen (65 %) parent-infant dyads scored below the 10th percentile on the total NCAFS score. Despite it being well-understood that parent-infant interaction is related to sociodemographic factors and parental mental health, there were no relationships between these factors and NCAFS scores in this study. Dyads who received enhanced parent education (n = 15) had lower NCAFS scores than dyads receiving usual care (n = 11) (p = 0.01).
Conclusion:
It remains unclear if the standard measure of parent-infant interaction, NCAFS, captured positive and negative interactions in context of assessment of a high-risk dyad within the NICU setting. The utility of the NCAFS with preterm infants in the NICU was not supported by this study.
Keywords: Premature infant, Human development, Parents, Interactions
1. Introduction
Parent-infant interaction can be conceptualized as a reciprocal, transactional activity that requires active participation from both parties [1]. Parent-infant interaction depends on the responsiveness and the affect displayed by each member of the dyad, caregiver sensitivity to the infant, caregiver availability to interact (related to emotional state, stress, and mental health), and the infant's ability to regulate their arousal state and provide clear cues for engagement or disengagement [2-4]. Infants depend on their caregiver for interaction which aids in the development of cognitive, language, social-emotional, and motor skills as well as secure attachment styles [2,5]. Parent-infant interaction can be influenced by a multitude of sociodemographic factors such as maternal age, education level, income, race, marital status [6], parent gender [7], and psychosocial factors such as maternal depression and anxiety [5]. However, parenting a full-term infant after birth differs from parenting a very preterm infant, with the NICU experience likely further impacting parent-infant interaction patterns [8-10].
Although parent-infant interaction can be observed early after birth when the full-term infant demonstrates a clear preference for eye contact with mutual, direct gaze [11], parents of very premature infants may experience early interactions in the NICU setting under unique circumstances which can include infant medical fragility, instability, and immaturity. Many very preterm infants (≤32 weeks estimated gestational age (EGA)) are initially separated from their parents and placed in incubators which also form a physical barrier between parent and infant [12]. Minimal handling may be prescribed as a neuroprotective measure within the first days after birth [13], further limiting early interactions. Additionally, the chaotic and stressful NICU environment, mixed with the parent's need to balance engagement with medical interventions aimed at sustaining life, must also be considered as potential factors that may impact parent-infant interaction [14] within the NICU setting.
Due to infants' need for specialized equipment and caregiving practices in the NICU, parents may feel disempowered and excluded and have difficulty establishing their parental identities, caregiving roles, and routines while their infant is hospitalized in the NICU [15-20]. In addition, parents may experience a myriad of emotions related to their infant's premature birth and medically fragile state that may influence their ability to engage with the infant [14,17,21]. Although there are environmental circumstances that can alter early parent-infant interaction among preterm dyads, caregivers may also appropriately limit interaction with their infant as a method to protect the infant from perceived stressful stimuli, which is a common aspect of neurodevelopmental care [22].
Programming aimed at fostering positive interactions between parents and their older infants and children may be different from education that parents recieve in the NICU. Education in the NICU largely consists of teaching parents to read and respond to the physiological and behavioral cues of their preterm infants to assist them in tailoring their interactions with their fragile infants [23]. This enhanced parental education related to appropriate interactions in the NICU has been found to increase the sensitivity and contingency responses of mothers with preterm infants in the NICU [24] and improve maternal knowledge and responses to infant cues [24,25]. This difference in expected parent responses in context may make early parent-infant interaction assessment in the NICU a challenge.
Some observational tools to assess parent-infant dyadic interaction during a typical daily activity (like play or feeding) include the Parent-Child Interaction (PCI) scale, the Nursing Child Assessment Feeding (NCAFS) and Teaching Scales (NCATS), Coding Interactive Behavior (CIB), Parent-Child Early Relational Assessment (PCERA), and the Emotional Availability Scales [26,27]. They largely consist of observations of caregiver sensitivity, dyadic communication, contingency of responses, and the synchrony between the dyad [27]. All of the aforementioned assessments have been validated for use in a home or clinic environment, from birth (term age implied) with various upper age limits from 24 months to 13 years [26,27]. There are also measures specifically designed to evaluate constructs closely related to parent-infant interaction, such as infant neurobehavior (Neonatal Behavioral Assessment Scale) and tools to enhance dyadic interaction (Newborn Behavioral Observation System) [28]. Still other tools aim to determine robustness of response related to environmental stimuli or caregiving activities (as in the Naturalistic Observation of the Newborn as part of the Newborn Individualized Developmental Care Assessment Program (NIDCAP) [29].
To our knowledge, none of the existing tools were specifically designed to only assess parent-preterm-infant interaction in the NICU. However, the NCAFS feeding scale can be used from birth onward, and one study used it to compare differences in interaction in the NICU in a small sample of parents who received enhanced parental education vs standard of care [24]. In this study, lower scores were observed in dyads who received the enhanced education. The NCAFS is widely used in research and considers the important and overlapping dimensions of the child, the caregiver, and the environment for assessment of the interaction taking place during the feeding time [4]. The NCAFS was developed at the University of Washington School of Nursing by Dr. Kathryn Barnard and a research team “to study ways of measuring health and caregiving environments of infants and young children” (p. 3) [30]. Families with both term and preterm children were included in the development of the scales [30], with parent-infant interaction assessed after discharge from the hospital at 4 and 8 months during a feeding activity [31]. Furthermore, the scales have been used in a cohort of preterm infants at 6 weeks corrected age after NICU discharge, with discrimination of scores achieved - after a NICU based intervention [4].
To improve our understanding of NCAFS as a potential measure of parent-infant interaction in the NICU, we investigated relationships between NCAFS scores in the NICU setting and 1) socio-demographic and medical factors, 2) parental mental health and confidence, and 3) enhanced parental education on reading and responding to infant cues (received as part of the Supporting and Enhancing NICU Sensory Experiences (SENSE) program). Understanding how these factors do or do not relate to measures of parent-infant interaction in the NICU can aid our understanding of this construct during the time in the NICU and lead to future scientific inquiry.
2. Methods
The study site institutional review board (IRB) at Washington University in St Louis, MO approved this study, and parents signed informed consent. There was also a ceded review at the University of Southern California (ceding oversight to the original study site at Washington University). The sample size was predetermined, as this study was nestled in an overarching study [32]. In the overarching study, 70 parent-infant dyads of preterm infants born ≤32 weeks EGA were enrolled within 7 days of birth and randomized to the SENSE program or standard of care to evaluate differences in parent and infant outcomes related to the SENSE program. The SENSE program included enhanced education on how to read and respond to the infant's cues in the NICU during sensory interactions, and such study enabled between-group comparisons related to the enhanced education for the current study. Further, in the cohort, medical, sociodemographic, and parent mental health factors were collected. Near term equivalent age, infants had a video recording of the parent feeding their infant, which allowed for scoring of a parent-infant interaction assessment, the NCAFS. This information was used to determine relationships between factors known to be associated with parent-infant interaction and NCAFS scores among the whole sample.
Twenty-six (37 %) of the enrolled sample had a video recorded (of adequate quality to enable assessment) of the parent feeding the infant. Videos were recorded between 34 and 48 weeks postmenstrual age (PMA) at the bedside in the NICU. The recording occurred as early as 34weeks, to capture infants who were discharged early, but as late as 48weeks for infants who had longer NICU stays. The variability of PMA near the time of NICU discharge is consistent with clinical practice and other research studies and was also documented. Videos were conducted to evaluate feeding performance and to assess parent-infant interaction. Videos consisted of the infant's mother or father feeding the infant, as decided by the parents, with no exclusions based on gender. It is acknowledged that parent-infant interaction may be impacted by a multitude of factors, which may include gender of the parent [33,34], but the research team aimed for inclusivity. Reasons for failure to achieve a video before discharge that could be used for assessment of parent-infant interaction included a lack of readiness to orally feed (medical complexity), challenges in coordinating the availability of parents to conduct feeding while the research team was available, and inadequate visibility of the dyads for assessment. Parents were instructed to feed their infants as they normally would, based on their experiences or recommendations from the NICU team. The video recording was started before the nipple entered the infant's mouth and stopped after full volume intake or if the parent indicated that the infant was not tolerating or was no longer engaged in the feeding. Parent-infant interaction was evaluated using the video recordings of the parents orally feeding their preterm infants in the NICU.
2.1. Parent-infant interaction: the NCAFS
The NCAFS was selected to assess parent-infant interaction as it can be used from birth to 12 months of age (with scoring tailored for infants from 1 to 5 months and 6 to 12 months respectively), it defines parent-infant interaction during feeding (a common activity in the NICU) [30], and it has previously been used with preterm infants [24]. The NCAFS is comprised of 76 total items that are divided into six subscales (four that address the caregiver and two that focus on the infant). The caregiver scales consist of 50 items and include: sensitivity of cues (16 items), response to distress (11 items), social-emotional growth fostering (14 items), and cognitive growth fostering (9 items). The infant scales consist of 26 items and include: clarity of cues (15 items) and responsiveness to caregiver (11 items). Embedded within these items are a total of 18 contingency items (15 for the caregiver and 3 for the infant scales). Contingency items capture behaviors when one person in the dyad triggers a reciprocal response from the other. Norms, based on infant behavior from 1 to 5 months, are provided that determine if a dyad scores ≤ the 10th percentile for interaction [30]. Within the manual, these cut-off scores are delineated for several ethnic groups [30]. One study was identified that specifically used the NCAFS assessment in the NICU with preterm infants born at or before 36 weeks EGA. They found that parents who received education on infants behavioral cues had more sensitive and contingent responses than parents in a control group, after reversing the scores [24] (meaning they considered low scores better performance and considered high scores to be worse performance, which is opposite to that described in the manual and training). However, the majority of research with the NCAFS involves parent-infant dyads in the home or clinic environment [27]. It has established reliability (with Cronbach's α = 0.86 for the combined total score), and various studies have been undertaken to establish content, criterion, and concurrent validity [30]. For this study, videos of parents feeding their infant were scored using the NCAFS by a trained and certified NCAFS instructor (author, KF).
2.2. Medical and sociodemographic factors
Medical and sociodemographic factors were collected from the electronic medical record, a discharge questionnaire, or through documentation by the research team. Infant medical factors included EGA (the number of weeks from the mother's last menstrual period until birth), PMA (EGA + number of weeks since birth) at assessment and discharge, birth weight, Apgar scores at 1 and 5 min, mode of delivery (Caesarean section, vaginal), whether the infant was part of a multiple birth, number of days on total parenteral feeding (TPN), number of days on a ventilator or noninvasive mechanical ventilation, as well as whether the infant had retinopathy of prematurity (ROP; any stage), patent ductus arteriosus (PDA; treated with indomethacin or surgical ligation), sepsis, necrotizing enterocolitis (NEC; all stages), or a significant brain injury (periventricular leukomalacia (PVL) or intraventricular hemorrhage (IVH) grade 3 or 4). Sociodemographic factors that were collected included infant sex, race (Caucasian/White; not Caucasian/White), maternal age, maternal marital status (legally married, not legally married), maternal education (some college or college education; no college), maternal employment status (currently employed, not employed), annual household income (categorized as below $25,000; $25,000–$49,999; $50,000–$99,999; $100,000–$149,999; $150,000–$200,000; above $200,000, dichotomized for reporting as <$25,000; >$25,000 based on the parent-reported income), insurance type (private or public), and child living situation (living with both parents, not living with both parents). These factors were investigated as it is understood that sociodemographic factors may impact parent-infant interaction [6]. Further, it would be anticipated that medical factors may relate to parent-infant interaction, as parent-infant interactions may be more tenuous when the infant is more premature or requires more medical support [4].
2.3. Mental health and confidence measures
Parents completed several measures related to mental health and confidence before discharge via a questionnaire. Total scores of the State-Trait Anxiety Inventory for adults-state and trait subscale (STAI) [35], Edinburgh Postnatal Depression Scale (EPDS) [36], Parental Stress Scale (PSS) [37], Parental Stressor Scale NICU (PSS NICU) [38], Parenting Stress Index – life stress subscale, 4th edition (PSI) [39], modified Perinatal Post-traumatic Stress Disorder Questionnaire (PPQ) [40], and Maternal Confidence Questionnaire (MCQ) [41] were calculated.
The psychometric properties of the abovementioned assessments have been established. The STAI has good reliability with Cronbach's α ranging from 0.87 to 0.92 [35]. The EPDS has satisfactory validity and good reliability with a standardized α = 0.87 [36]. The PSS has adequate internal reliability with α = 0.83 and a test-retest coefficient at 0.81 [37]. The PSS NICU has good reliability overall (α = 0.89) [38], as does the PSI (α = 0.96) [39]. The PPQ has good test-retest reliability, internal reliability, and internal consistency (α = 0.90) [40]. The MCQ also has acceptable test-retest reliability (0.69) and Cronbach's α = 0.89 [41]. Measures of parent mental health and confidence were collected to determine their relationships with parent-infant interaction in the NICU, because parental mental health challenges and confidence have been related to parent-infant interaction [3,5,42].
2.4. Enhanced education in NICU
Infants were randomized in the overarching study to standard of care or enhanced education (provided through the SENSE program). Both groups received standard of care, which included routine parent education by therapists, nurses, and other health care professionals on appropriate interaction with their infant. In addition, the enhanced education group received a booklet containing parent-education materials shortly after birth. The booklet covered a range of topics related to the SENSE multisensory program with a chapter dedicated to how to recognize and interpret the infant's behavioral cues to assist parents in identifying when to give the infant a break, when to help them cope with stressors, and when to interact based on signs of readiness. This education pertained specifically to periods during which the parent and infant dyad were engaged in positive multisensory experiences such as skin-to skin holding, rocking, and face to face interaction. In addition to the parent education materials, a neonatal therapist facilitated a verbal parental education session within one week of study enrollment, and weekly follow-up visits occurred to revise and engage with parents around the concepts contained in the booklet [32]. Such education related to reading and responding to infant cues is considered optimal or enhanced education in the NICU to facilitate appropriate parent-infant interactions. Whether parents were randomly assigned to the enhanced education as part of the multisensory programming (SENSE program) or assigned to usual care was documented to aid in determining differences in NCAFS scores based on type of education provided in the NICU.
2.5. Statistical analysis
Descriptive statistics were used to report NCAFS scores among very preterm parent-infant dyads (≤32 weeks EGA) in the NICU. Outcomes were investigated for normality and equal variances. Although all other analyses investigated the relationships between each independent variable (medical, sociodemographic, and parent mental health) on the NCAFS scores, a between-group design was used to evaluate the impact of enhanced education (with assignment into groups being through randomization in the overarching study). We investigated relationships between medical and sociodemographic factors and NCAFS scores using independent samples t-tests or linear regression models. Linear regression models were also used to investigate relationships between parent mental health and confidence and NCAFS scores. Finally, we investigated differences in NCAFS scores among those who did and did not receive the enhanced education using independent samples t-tests. Significance was defined as p<0.05. We also re-ran analyses excluding fathers to determine if this changed the findings.
3. Results
Twenty-six parent-infant dyads (23 mother-infant dyads and three father-infant dyads) were included in the analyses. The average PMA at the time of assessment was 38.7 ± 3.6 weeks. The duration of the feeding recordings that were used in analysis ranged from 5 min to 28 min (mean: 15:24 ± 4:59).
The mean ± standard deviation of the total NCAFS score was 46.9 ± 9.3 with 17/26 (65 %) dyads scoring below the 10th percentile. The mean ± standard deviation of the parent total NCAFS score was 33.8 ± 6.4, with 14/26 (54 %) parents scoring below the 10th percentile. The mean ± standard deviation of the child total NCAFS score was 13.1 ± 4.5, with 13/26 (50 %) infants scoring below the 10th percentile. The mean ± standard deviation of the contingency total score was 10.4 ± 3.2 (there are no cut-offs for the 10th percentile). All NCAFS outcomes were normally distributed. Two NCAFS subscales (socio-emotional growth fostering and infant clarity of cues) did not have equal variances between the standard of care and enhanced education groups, therefore, analyses that accounted for unequal variances were used. All other NCAFS outcomes had equal variances between groups.
Table 1 documents the medical and sociodemographic characteristics for the 26 parent-infant dyads in the sample and the p-values from investigating the relationships of those factors to NCAFS scores. Infants with public insurance scored lower on the infant total score (t (24) = −2.6, CI: −7.4; −0.8, p = 0.02). There were no other significant relationships between infant medical or sociodemographic factors and NCAFS scores.
Table 1.
Sociodemographic and medical characteristics of the sample (N = 26) and relationships to NCAFS scores.
| Total Mean (±SD) or N (%), Median (IQR) |
NCAFS total score p-value |
Parent total score p-value |
Infant total score p-value |
Contingency score p-value |
|
|---|---|---|---|---|---|
| EGA | 30.0 (±2.4) | 0.73 | 0.60 | 0.97 | 0.62 |
| PMA at assessment | 38.7 (±3.6) | 0.62 | 0.91 | 0.39 | 0.96 |
| PMA at discharge | 39.8 (±3.7) | 0.58 | 0.84 | 0.39 | 0.99 |
| Infant sex: male | 13 (50.0 %) | 0.52 | 0.95 | 0.15 | 0.76 |
| Infant race: Caucasian/White | 19 (73.1 %) | 0.88 | 0.77 | 0.91 | 0.90 |
| Birth weight (g) | 1493.3 (±505.4) | 0.42 | 0.45 | 0.57 | 0.26 |
| APGARS at 1 | 3.7 (±2.9) | 0.56 | 0.32 | 0.83 | 0.35 |
| APGARS at 5 | 5.9 (±2.1) | 0.76 | 0.71 | 0.91 | 0.34 |
| CRIB II score | 4.0 (IQR: 0–8) | 0.74 | 0.87 | 0.36 | 0.76 |
| Multiple birth | 12 (46.2%) | 0.99 | 0.58 | 0.41 | 0.54 |
| Mode of delivery: C-section | 23 (88.5 %) | 0.54 | 0.95 | 0.48 | 0.81 |
| Number of days on TPN | 5 (IQR: 0–8) | 0.41 | 0.41 | 0.61 | 0.93 |
| Days on ventilator | 1 (IQR: 1–11) | 0.84 | 0.98 | 0.65 | 0.85 |
| Days on NIMV | 6 (IQR: 3–19) | 0.89 | 0.50 | 0.49 | 0.58 |
| ROP | 5 (19.2 %) | 0.13 | 0.17 | 0.25 | 0.63 |
| PDA | 5 (19.2 %) | 0.26 | 0.41 | 0.25 | 0.87 |
| Sepsis | 4 (15.4 %) | 0.71 | 0.99 | 0.44 | 0.58 |
| NEC | 1 (3.8 %) | 0.20 | 0.37 | 0.17 | 0.90 |
| Significant brain injury (PVL/IVH Grade3/4) | 2 (6.7 %) | 0.65 | 0.58 | 0.91 | 0.98 |
| Maternal age | 29.3 (±7.0) | 0.54 | 0.56 | 0.66 | 0.37 |
| Maternal education (Some college or higher) | 20 (77.0 %) | 0.33 | 0.12 | 0.87 | 0.22 |
| Currently employed | 10 (38.5%) | 0.11 | 0.16 | 0.21 | 0.22 |
| Annual income <$25,000 | 11 (42.3 %) | 0.44 | 0.48 | 0.56 | 0.31 |
| Insurance type (Public) | 13 (50 %) | 0.19 | 0.77 | 0.02 t(24) = −2.6 CI: −7.4; −0.8 | 0.59 |
| Marital status (Legally married) | 15 (57.7%) | 0.88 | 0.85 | 0.98 | 0.77 |
| Child lives with both parents | 19 (73.1 %) | 0.60 | 0.53 | 0.86 | 0.59 |
EGA: estimated gestational age, PMA; postmenstrual age, CRIB: clinical risk index for babies, TPN: total parenteral nutrition, NIMV: noninvasive mechanical ventilation, ROP: retinopathy of prematurity, NEC: necrotizing enterocolitis, PVL: periventricular leukomalacia, IVH: intraventricular hemorrhage, NCAFS: Nursing Child Assessment Feeding Scale.
p-values are from investigating relationships between medical and sociodemographic factors and NCAFS scores using independent samples t-tests and linear regression models. Bold p-values indicate statistical significance (p < 0.05); T-statistic and CI: 95 % Confidence Interval only reported for significant p-values (p < 0.05).
Table 2 documents p-values from investigating relationships between parent mental health, confidence, and NCAFS scores. There were no relationships observed between parent mental health and confidence measures and NCAFS scores.
Table 2.
Relationships between parent mental health and confidence measures and NCAFS scores.
| Factor | NCAFS total score p-value |
Parent total score p-value |
Infant total score p-value |
Contingency score p-value |
|---|---|---|---|---|
| Parenting Stress Scale | 0.77 | 0.96 | 0.62 | 0.99 |
| Edinburgh Postnatal Depression Scale | 0.25 | 0.39 | 0.31 | 0.44 |
| State Trait Anxiety Inventory (state) | 0.15 | 0.34 | 0.15 | 0.37 |
| State Trait Anxiety Inventory (trait) | 0.33 | 0.59 | 0.25 | 0.40 |
| Parental Stressor Scale NICU | 0.18 | 0.13 | 0.57 | 0.09 |
| Parenting Stress Index (stress score total) | 0.86 | 0.57 | 0.63 | 0.68 |
| Perinatal Posttraumatic Stress Disorder Questionnaire | 0.22 | 0.37 | 0.28 | 0.24 |
| Maternal Confidence Questionnaire | 0.84 | 0.92 | 0.79 | 0.61 |
p-values are from investigating relationships between parent mental health and confidence measures and NCAFS scores using linear regression models. NCAFS: Nursing Child Assessment Feeding Scale.
Table 3 defines the differences in NCAFS scores among dyads who did (n = 15) and did not (n = 11) receive the enhanced education. Parents who received the enhanced education had lower total scores for the NCAFS (across both infant and parent subscales) (t (24) = 2.8, CI: 2.3–15.8, p = 0.01), lower total scores on the parent subscales (t (24) = 3.1, CI: 2.3–11.4, p = 0.005) as well as lower scores for sensitivity to their child's cues ((t (24) = 3.0, CI: 0.8–4.3, p = 0.007), socio-emotional growth fostering ((t (23.1) = 3.6, CI: 1.1–4.1, p = 0.002) and cognitive growth fostering ((t (24) = 3.6, CI: 0.9–3.40 p = 0.001). No differences were observed in infant subscale scores.
Table 3.
Differences in NCAFS Scores among the dyads who received usual care or enhanced education while in the NICU.
| NCAFS subscale | Total (n = 26) Mean (±SD), range |
Usual care (n = 11) Mean (±SD), range |
Enhanced education (n = 15) Mean (±SD), range |
t-Statistic t(24)= |
Confidence interval | p-value |
|---|---|---|---|---|---|---|
| NCAFS total score, range 0–76 | 46.9 (±9.3) | 52.1 (±7.9) | 43.1 (±8.5) | 2.8 | 2.3; 15.8 | 0.01 |
| 31–64 | 36–64 | 31–60 | ||||
| NCAFS parent total, range 0–50 | 33.8 (±6.4) | 37.7 (±5.1) | 30.9 (±5.8) | 3.1 | 2.3; 11.4 | 0.005 |
| 21–43 | 6–43 | 21–42 | ||||
| NCAFS sensitivity to child cues, range 0–16 | 11.3 (±2.5) | 12.7 (±1.9) | 10.2 (±2.3) | 3.0 | 0.8; 4.3 | 0.007 |
| 6–15 | 9–15 | 6–14 | ||||
| NCAFS response to child distress, range 0–11 | 10.0 (±1.5) | 9.7 (±2.0) | 10.1 (±1.0) | −0.7 | −1.6; 0.8 | 0.49 |
| 5–11 | 5–11 | 8–11 | ||||
| aNCAFS social emotional growth fostering, range 0–14 | 9.2 (±2.3) | 10.6 (±1.4) | 8.1 (±2.3) | t(23.1)=3.6 | 1.1; 4.1 | 0.002 |
| 4–12 | 8–12 | 4–12 | ||||
| NCAFS cognitive growth fostering, range 0–9 | 3.4 (±1.8) | 4.6 (±1.2) | 2.5 (±1.7) | 3.6 | 0.9; 3.4 | 0.001 |
| 0–6 | 3–6 | 0–5 | ||||
| NCAFS child total, range 0–26 | 13.1 (±4.5) | 14.4 (±4.0) | 12.2 (±4.8) | 1.2 | −1.5; 5.8 | 0.23 |
| 6–21 | 10–21 | 6–19 | ||||
| aNCAFS clarity of cues, range 0–15 | 8.8 (±2.8) | 9.6 (±2.1) | 8.3 (±3.1) | t(23.8)=1.3 | −0.8; 3.4 | 0.22 |
| 4–13 | 7–13 | 4–13 | ||||
| NCAFS responsiveness to caregiver, range 0–11 | 4.3 (±2.1) | 4.8 (±2.2) | 3.9 (±2.0) | 1.1 | 0.30 | |
| 1–9 | 2–9 | 1–9 | ||||
| NCAFS contingency total, range 0–18 | 10.4 (±3.2) | 11.4 (±3.4) | 9.7 (±2.9) | 1.3 | −0.9; 4.2 | 0.20 |
| 3–16 | 3–16 | 5–15 |
NCAFS: Nursing Child Assessment Feeding Scale. p-value is from investigating differences in mean NCAFS scores among those who did and did not receive the enhanced education using independent sample t-tests. Bold p-values indicate statistical significance (p < 0.05).
Levene's test for equality of variance was significant and therefore equal variances were not assumed on these outcomes. Equal variances were assumed on all other outcomes.
After re-running the analyses, excluding the 3 father-infant dyads in the sample, our findings remained largely unchanged, and therefore the result for the entire sample is reported.
4. Discussion
The key findings of this study were that 1) there were no relationships between infant medical or sociodemographic factors and NCAFS scores, despite the anticipated influence of such factors on parent-infant interaction, 2) there were similarly no relationships between parental mental health and confidence and NCAFS scores, and 3) poorer scores on the NCAFS were observed among dyads who received what was deemed as enhanced education in the NICU. Anticipated relationships with parent-infant interaction were not observed, and in some cases went in the opposite direction. Therefore, the use of measures such as the NCAFS in the context of high-risk infants in the NICU setting to define parent-infant interaction was not supported in this study and requires further inquiry. In addition, investigation into the components of existing parent-infant interaction measures and evaluation of their relevance to the NICU setting may be needed. Further, parent-infant interaction measures that are specifically designed for assessment of the high-risk dyad in the NICU setting may need to be developed.
A large proportion of our total sample, 17 (65 %) dyads, scored below the established 10th percentile cut-off scores on the NCAFS. In addition, 6 (23 %) parents scored below the 10th percentile cutoff, while their infant scored above the cutoff (an observation that indicates that although the preterm infant may have been showing adequate interaction cues and responsiveness, the reciprocal responsiveness, socio-emotional, and cognitive growth fostering expected from the parent was diminished). It is unclear if this represents a large number of parents with poor parent-infant interaction, or if parent-infant interaction in the NICU is different than at other stages of development or in other settings, potentially inflating parent-infant interaction challenges observed in this population.
The findings of this study warrant further discernment as to whether ‘appropriate’ parent-infant interaction in the NICU may be different from ‘appropriate’ parent-infant interaction during other developmental stages and in the home or clinic environment. As such, it is unclear if the current measures of parent-infant interaction in the NICU are measuring what is intended, or if new measures of parent-infant interaction specifically designed for NICU dyads would yield similar results. It should be noted that the NCAFS is designed for infants from birth (term age implied) to 12 months, with the scoring used for our study based on interaction with infants from 1 month to 5 months.
Feeding is a crucial activity within the NICU that may promote parent-infant closeness, bonding, intimacy and parental role fulfillment [12,43]. Feeding time can therefore play an integral role in parent-child interaction patterns. During the first few weeks of life after a full-term birth, feeding naturally occurs numerous times, and it is assumed that both the parent and infant would be comfortable and competent to engage in simultaneous social interaction while feeding [30]. However, in the NICU parenteral feeding or nasogastric/orogastric feeds may be prescribed, and parents may not consistently have the opportunity to engage directly in the caregiving activity of feeding, which can be a significant source of stress [44,45]. In addition, once infants are ready to feed orally, they may have altered feeding experiences due to their immature feeding skills, limiting their comfort and interaction abilities during feeding, and may require feeding interventions focused on biomechanical support such as pacing, positioning, etc. [46]. Further, it has been demonstrated that feeding of preterm infants at term age is different from feeding full-term neonates [46]. Feeding challenges (such as maintaining an appropriate level of arousal, coordinating suck-swallow-breathe synchrony, and managing decreased oral motor tone) are common in preterm populations during their NICU stay and may persist when infants reach term equivalent age [46]. Such challenges can impact interactions during feeding. Parents in this study were instructed to feed the infant as they normally would, and several parents positioned the infant in side-lying. Emerging evidence indicates that this position may enhance the infants' physiological stability during feeding [47]. However, this position directly precludes several items on the NCAFS such as achieving trunk-trunk contact between the dyad (NCAFS item 3, sensitivity to cues subscale) or being in the “en-face” position to engage in eye contact (NCAFS item 29, socio-emotional growth fostering subscale). Parents may have been focused on optimal positioning and safe feeding practices rather than focusing on facilitating social interaction. Positioning and feeding recommendations may therefore have a direct impact on the feeding process and NCAFS scoring.
Preterm infants also show variation in neurodevelopmental behavior at term age as compared to full-term infants [48]. These differences include lower scores on handling in addition to decreased selfregulation, orientation, and changes in stress and excitability [48]. These factors may further influence the infant's ability to initiate clear cues and responsively engage with the parent while feeding. Moreover, several items on the NCAFS require skills that are not developmentally appropriate during the early neonatal period, such as smiling or laughing, active exploration, and responding to social games which may have further impeded the dyads' performance on the standard measure.
The lack of associations between medical and sociodemographic factors and NCAFS scores in the current study is inconsistent with other studies. Previous research has found that neonatal medical risk factors, such as complex medical diagnoses or prematurity, are related to challenges in dyadic interaction [14,49] with prolonged family effects, stress, and intrusive parenting practices noted by several authors [50]. Further, socioeconomic risk has been described as a contributor to poorer maternal-infant interaction [6]. However, our findings did not reveal the same relationships between medical or sociodemographic factors and parent-infant interaction when using the NCAFS in the NICU setting. Our finding of lower scores for infant interaction based on insurance type should not be mistaken as an indication of poorer parent-infant interaction, as the finding only related to infant behavior and was not significant across NCAFS total scores or subscales.
Additionally, the absence of relationships between parent mental health and confidence and NCAFS scores differs from other studies that describe poorer mother-infant interaction among parents who are stressed, anxious, depressed, or who lack confidence in their parenting abilities [3,5,41,51]. The “serve and return” parent-infant relationship is critical to the developing infant brain and the absence of consistent, child-focused responsive attention may lead to developmental delays [52]. In addition, maternal verbal interaction has been shown to have beneficial effects in terms of regulating preterm infant autonomic and physiological responses and maternal anxiety in the NICU [53]. Our group has previously observed less parent engagement in the NICU among parents who have high levels of stress and lower confidence [54], and it would be expected that mothers with more depression, anxiety, and stress may show lower levels of engagement [30]. However, relationships between parent-infant interaction and parent mental health and confidence were not found in the current study.
Our findings of poorer performance on parent-infant interaction using the NCAFS measure among dyads with enhanced education were consistent with other reports [24]. Preterm infants can experience less verbal interaction from their parents presumably due to infant immaturity or lower arousal levels [30]. Even among infants with optimal selfregulation, their parent-infant interaction may differ from that of parent-infant dyads with full-term infants due to the education that parents receive about responding to infant stress cues while in the NICU. The SENSE program's enhanced education aids parents in reading and responding to their infant's cues to enable parents to engage in positive and appropriate multi-modal sensory experiences that are tailored to the infant's PMA and tolerance [32,55,56]. Parents in the enhanced education group may have been limiting their verbal input, rocking, and playful interaction during the complex feeding activity as an appropriate response to their infants' subtle behavioral cues and tolerance, resulting in lower NCAFS scores.
Recently, there have been calls to critically evaluate the appropriateness of several items on the NCAFS [57,58]. In line with these suggestions, it may be indicated to further evaluate the applicability of the items on the NCAFS to a preterm population within the NICU. NCAFS was not specifically designed for use in the NICU, and there are several items that may not fit the appropriate interaction or the environmental factors that commonly occur in the NICU. For example, the NCAFS measures multimodal interaction typical of older infants and their parents during the familiar activity of feeding, with several items (item 7, 8, 32, 34, 45, 46, 48, 49) on the scale directly related to the caregiver giving verbal input during the feeding activity. Additionally, items 9–11 on the sensitivity to cues scale calls for varied intensity of verbal input, touch, and rocking or movement [30]. If parents have been educated to provide only gentle, slow movement and to keep the environment relatively quiet during cares as an appropriate response to infant distress cues that are often seen with handling [59], the parents may not score well on these items despite interacting in a sensitive manner. Therefore, the parental omission of certain overt interactive actions among those who received the enhanced education may have been appropriate in context, given the neurodevelopmental immaturity of the preterm infants. Yet this may be captured on the NCAFS measure as a negative interaction, rather than a positive one. Previous researchers interpreted higher scores on the NCAFS as indicative of lower parental contingency, given the sensitivity of preterm infants to over stimulation in the NICU [24]. However, inverting the scoring of this measure may not optimally describe nuances in dyadic interaction, as some items may still be appropriate to score depending on the infant behavioral state during the feeding (i.e. items related to safe positioning for feeding, varying the pace of feeding or pausing in response to infant cues etc.).
This study has highlighted an interesting finding in that the expected sociodemographic, infant medical, and maternal characteristics were not related to parent-infant interaction scores on the NCAFS, while enhanced education was associated with scores in an unanticipated direction. The contextual factors of the NICU, along with education on reading and interpreting infant cues, may therefore have contributed to the poor scores observed and highlights the need for further consideration of assessments of parent-infant interaction in the NICU. Assessments of parent-infant interaction in the NICU should reflect the developmental stage of the infant, the activity completed, whether there might be other factors influencing the parent's responses during that activity, and the context of training that parents of infants undergo during NICU hospitalization. Therefore, the findings of this study do not support use of the NCAFS in the NICU setting, and further research is needed.
Parent-infant interaction within the NICU is a complex phenomenon, fraught with cultural, emotional, medical, and developmental considerations [14]. Given the complexity of the construct, flexible outcome measures that are responsive to cultural and contextual factors, rapid infant development, and variations in NICU best practice guidelines and recommendations, should be used. Future research could focus on developing a tool specifically designed for high-risk populations within the NICU. The tool needs to be sensitive to subtle infant cues and behavioral states when assessing neonatal infant interaction, consider infant neurobiological maturity, and reflect prior parental knowledge and instruction or education with regards to engagement during complex caregiving tasks. Further research is required to determine if feeding is an optimal activity to assess interaction within the NICU setting or if a less demanding parent-infant activity in the NICU may be more suitable to measure interaction to limit the confounding factors that may have impacted the current results. Clinicians may note that parental education to minimize multimodal interaction during complex tasks in the NICU might result in decreased parent-infant interaction during tasks such as feeding and may therefore guide parents to gradually increase interaction during routine caregiving practices as the infant's tolerance improves.
4.1. Limitations
This study had several limitations. The video recording equipment was relatively limited and could not accommodate changes in the position of either caregiver or infant, which hampered the analysis of dyadic interaction at times. Many videos could not be used due to poor quality or the visibility from the camera angle. During several recordings, visitors entered the infants' NICU rooms (either family or staff) that demanded the attention of the caregiver during the feeding, and this may have decreased parental scores on the NCAFS. This limitation is inherent in the NICU setting and should be factored into future test development. The video was one moment in time that may or may not be reflective of typical interactions and does not capture interactions that may occur during non-feeding times. In addition, parental behavior could have been influenced by the understanding that the interaction was being recorded. The enhanced education on interpreting and responding to infant cues were recommended for parents to apply during multimodal sensory activities, which could include caregiving activities- yet it was not specifically tailored to feeding activities as this was not the focus of the overarching study. There was no measure used to gauge parental knowledge on the education provided. Further, due to the small sample size, we were not able to distinguish differences in parent-infant interaction among mother-infant compared to father-infant dyads. By removing the 3 father-infant dyads, our findings remained largely unchanged. No follow-up measures of parent-infant interaction were obtained for this sample, and therefore it is not possible to conclude whether the low interaction scores were specific to the NICU context and infant prematurity or whether these dyads continued to exhibit low interactive engagement. The convenience sample was small and part of an overarching cohort with no power analysis for this study, therefore there is a risk of both type 1 and type 2 errors. These findings may not generalize to the broader NICU population.
5. Conclusion
Measurement of parent-infant interaction within the NICU environment with preterm infants is complex. The low NCAFS scores and lack of anticipated relationships of NCAFS scores with known medical, sociodemographic, and mental health factors in this small sample are of concern. It is also of concern that parents who received enhanced education on reading and responding to infant cues in the NICU had poorer scores on the NCAFS. The utility of the NCAFS in the NICU was not supported in this small study. There is a need for measures of parent-infant interaction that are specifically designed to assess high-risk parent-infant dyads in the NICU.
Acknowledgment
The authors wish to thank the infants and families who participated in this study. In addition, we would like to thank Bethany Gruskin, Carolyn Ibrahim, Delaney Smith, Jessica Roussin, Polly Kellner, Christa Thompson, Katie Harper, Kristen Connell, Tiffany Le, Mary Raney, Elizabeth Heiny Wedell, Anna Bukhshtaber, Mary Politi, Aimee James, Elizabeth Kruvand, and Sessions Cole.
Funding sources
Research reported in this publication was supported by the Gordon and Betty Moore Foundation, the Washington University Institute of Clinical and Translational Sciences grant UL1TR002345 from the National Center for Advancing Translational Institute of Health R01 HD 057098, and the Intellectual and Developmental Disabilities Research Center at Washington University (NIH/National Institute of Child Health and Human Development P30 HD062171).
Footnotes
Declaration of competing interest
Two of the authors (RP and JS) are authors of the SENSE program. The program is available ‘at cost’ to clinicians and researchers, with no financial benefit to the authors.
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