Pediatrician and parental evaluation of child neurodevelopment at 2 years of age

In the first few years of life, children reach numerous developmental milestones in various domains, acquiring cognitive, social, and emotional skills that will provide the foundations for their lifelong health and achievements [1, 2]. At the same time, exposure to environmental stressors can have negative long-term consequences for children’s early development [3]. Early interventions are crucial to prevent motor, cognitive, and emotional impairments.

Nowadays, there is an increase in formalized developmental screenings in primary healthcare towards detecting developmental disorders earlier [4]. The American Academy of Pediatrics [5] recommends screenings at different age stages, with attention to postpartum depression in mothers during the first year of life [6], to the identification of developmental disorders at 9–30 months, and the early identification of autism at 18–24 months [7]. Pediatricians are the first healthcare providers to advocate for infants and children’s health and safety [8‐10]. They monitor development and consider all aspects of a child’s well-being, including biological, social, and psychological factors [10]. There has been increasing effort to identify and intervene early in children with developmental disabilities or delays because it has been demonstrated that delayed diagnoses lead to missed opportunities for interventions known to decrease lifetime costs, reduce the chances of future developmental disorders, and prevent secondary sequelae [11, 12]. In monitoring neurobehavioral development, it is therefore fundamental to consider the shared perspectives of parents and pediatricians. Parents are the infants’ primary care environment and through clinical encounters with families, pediatricians can access all aspects of a child’s well-being, including biological, social, and psychological factors. The World Health Organization encourages establishing a close relationship between parents and healthcare providers in identifying infants with a risk for neurodevelopmental disorders and setting up early interventions [13]. Yet, there are currently no shared indications of joint parent-pediatrician assessments. In addition to promoting early identification of developmental problems, an emphasis on parents as essential sources of information on children’s health offers additional benefits [14].

One of the factors that can impact children’s well-being is parental heightened stress [15]. Parental stress (maternal or paternal) is typically experienced when the demands of the parenting role exceed coping abilities [16, 17]. Parents with higher parenting stress levels are more likely to see their children display more deficits in language, social, and cognitive skills [18, 19].

Mothers’ negative emotionality is linked with unsupportive parental responses and subsequent child behavior problems [20‐22]. Evidence such as this suggests that a negative maternal experience represents a risk factor for developing behavioral problems and neuropsychiatric disorders in infancy. A recent study [23] highlighted that parenting stress during infancy (11.4 ± 3.1 months) was significantly associated with mental health problems in 3-year-old children. Current views emphasize a multifactorial and multi-determined conception of parenting stress involving parent-related sources and individual distress [24‐26].

However, a bidirectional association between parenting stress and child functioning has been found, of which internalizing and externalizing behaviors were the primary interests [19]. A recent study reported bidirectional associations between parenting stress and child psychopathology (with children aged 5 to 9) at different levels of maternal affection [27]. Findings of a recent systematic review [28] indicated that healthcare professionals could intervene on some modifiable factors, such as parental depression and social support, through tailored support; this might guide the development of preventive interventions and strategies.

The aim of the present study was three-fold: (a) to test the feasibility of using parent-report instruments to detect warning signs in their children’s development; (b) to ascertain whether there is an agreement between the family pediatricians’ (FP) clinical judgments of children’s warning signs and the parental perceptions; (c) to determine whether there is a link between parents’ distress and child development.

Forty-eight FPs agreed to be involved in this sub-study, and 532 infants with their parents were recruited. Data concerning the follow-up assessment were available for 435 children (232 male and 203 female) included in the present study. No further information was collected for the other 97 toddlers due to the FPs’ retirement.

From either the FP assessment or the parental M-CHAT-R questionnaire, 69 toddlers (15.9%) presented warning signs. In particular, 33 children had warning signs only in the FP assessment, 26 only in the M-CHAT-R, and 10 in both assessments; 366 were not at risk. For the 69 toddlers with warning signs, associations with risk and protective factors were analyzed to identify possible markers of risk conditions (Table 1). In the univariate analysis, being male (OR 1.94, 95% CI 1.13–3.32) or having at least one foreign-born parent (OR 2.13, 95% CI 1.06–4.26) were significant risk factors. On the other hand, protective factors were reading aloud (not exposed vs. exposed: OR 2.93, 95% CI 1.72–4.97) and spending at least one hour per day outdoors (not exposed vs. exposed: OR 2.08, 95% CI 1.23–3.51). The logistic regression analysis confirmed being male (OR 2.46, 95%CI: 1.23–4.91) as a factor associated with a greater likelihood of warning signs, in addition to having sleep disorders (OR 2.43, 95% CI 1.17–5.04), while reading aloud was confirmed as a protective factor, with children not exposed versus exposed having an OR = 2.98 (95% CI 1.54–5.78).

Follow-up revealed that among the 69 toddlers with warning signs, 26 were referred for further evaluation to a neuropsychiatrist or psychologist. In addition, 7 of the toddlers who did not present warning signs were also referred. Out of 33 children who underwent a specific clinical evaluation, 16 received a diagnosis (of whom 14 had warning signs and 2 did not): language disorders (n = 9), autism (n = 3), developmental delays (n = 2), and other conditions (n = 2). For the M-CHAT-R, a sensitivity of 62.5% (95% CI 35.4–84.8%) and a specificity of 76.5% (95% CI 50.1–93.2%) were calculated. For the FPs’ assessments, a sensitivity of 75.0% (95% CI 47.6–92.7%) and a specificity of 41.2% (95% CI 39.7–75.0%) were estimated. Combining the M-CHAT and FP assessments, we observed a sensitivity of 87.5% (61.7–98.4%) and a specificity of 29.4% (95% CI 10.3–56.0%).

The follow-up assessment was completed for 435 infants, of whom 69 (15.8%) presented warning signs. Being male and having sleep disorders was associated with a greater likelihood of warning signs in the multivariate analysis, while reading aloud was a protective factor. For 73 children (18.4%), at least one parent tested positive for PSI-SF; an increased prevalence of parental distress was observed in children with warning signs.

Although a few recent studies have highlighted the importance of a shared approach between parents and pediatricians in screening and encouraging early diagnoses [7, 42‐44], the present study is the first to integrate the parental and FP perspectives to detect those children with possible warning signs early. The feasibility of integrating the FPs and parental perspectives was confirmed. In our cohort, 1 out of 6 children was considered “at risk” at the FP assessment (10.1%), the parental M-CHAT-R questionnaire (8.3%), or both. Similar percentages were found in several international studies that used the CDC [45] or the M-CHAT-R questionnaire [46‐49]. The combined risk percentage assessed in this study was indeed higher, precisely 16%. The pediatricians, however, did not consider a psychiatric or psychological evaluation essential for most of these children. Because approximately 1 out of 20 children were referred for further evaluation, this proportion was consistent with previous literature [47].

Only for 10 out of 69 children the warning signs were reported by both parents and FPs. This number was expected since the tools (M-CHAT-R and CDC checklist) evaluate different skills and domains. It should be underlined, however, that the agreement between parents and pediatricians was low when considering the six overlapping questions in the M-CHAT-R and the CDC questionnaires (considering pretend play, climbing onto furniture, pointing, walking, copying others, and following orders). This observation converges with the idea that parents and FPs may have different perceptions of the warning signs and that a shared approach is needed, as documented by the increase in sensitivity when combining the two evaluations.

Consistent with the findings of other studies [50‐52], signs of potential neurodevelopmental disorders resulted more frequently in males. An Indonesian study [53] used the M-CHAT-R to screen children aged 16–30 months and showed that 3.5% of the subjects were at high risk of developing ASD; only the male gender was significantly associated with ASD. The male-to-female ratio with moderate-to-high-risk M-CHAT-R results was 2.5:1. Similarly, a male-female ratio of 2:1 exists among individuals with intellectual disability/developmental delay [54] and a 4:1 ratio for individuals with autism diagnoses [55]. Moreover, an association between sleep disorders in children and developmental disorders, such as pervasive developmental disorder (PDD) and attention deficit hyperactivity disorder (ADHD), was detected [56, 57]. Having at least one foreign parent was also associated with an increased likelihood of having warning signs. Some aspects, in particular socio-demographic variables (e.g., parental level of education, and parental nationality) could indicate other significant factors that might directly impact on children warning signs and development. Parental race, ethnicity, and culture can affect child development. Parent-child relationships and parental behavior affect children’s health and well-being across ethnicities, cultures, and genders in traditional as well as nontraditional families. Present findings are consistent with reported more specific and appropriate evaluations, suggesting an in-depth analysis in future studies [58, 59]. On the other hand, in the present study reading aloud and spending at least one hour per day outdoors were protective factors: parents whose infants had a lower likelihood of warning signs were more adherent to those actions embedded in the nurturing care concept. Previous studies describe both these factors as having a protective role in neurodevelopment [60, 61].

From the parental assessment, almost one out of five children was observed to have one parent with clinically significant distress. Considering the children “at-risk,” this percentage rose to nearly one-third. The prevalence of parental distress was similar in mothers and fathers. In the literature, parents of a non-clinical sample reported a lower prevalence of stress, i.e., between 7 and 9% [62, 63]. It is important to highlight that no recent studies report updated estimates. Therefore, several factors (e.g., the COVID-19 pandemic, financial difficulties, and the environmental crisis) might have determined increased stress levels. Fewer studies involving parents of children and adolescents with neurodevelopmental disorders have reported high-stress levels in their parental role [64]. An association was also found between the presence of warning signs in infants and parental stress in mothers, while the same was not confirmed in fathers. The same gender difference was previously reported when evaluating parents of children with other clinical conditions [65]. Research has shown that the relationship between child behavioral problems and parental stress is bidirectional [66]. Since parental stress data have been collected only when child was 24 months, it is impossible to verify if it is antecedent or consequent to the child’s difficulties. It has been tested whether there was a difference in parental stress considering delivery child in pandemic times but, although literature shows that there was an increase in parental stress during pandemic time in Italy [67] the results if the present study found no differences at 24 months visit between parents of children born before or after pandemic time. Parents with poorer psychological well-being may perceive their child’s behavior more negatively. At the same time, parental distress may interfere with the parent’s ability to remain sensitive and accepting of the child [68]. Those children might, therefore, receive less protective actions such as reading aloud and spending time outdoors.

Some limitations must be considered. Even if neurodevelopmental disorders may be recognized at 18 months, the assessment was scheduled at 24 months consistently with the timing of well-child visits in most Italian regions. Therefore, in a few cases, the warning signs may have been present earlier. Moreover, the FPs involved participated voluntarily and might not be fully representative of all Italian family pediatricians. The COVID-19 pandemic represented a challenge for the NASCITA cohort study and may have impacted parents’ and children’s well-being. We included the period of birth (pre-pandemic vs. first wave) among the covariates, which did not influence the likelihood of developing warning signs or parental stress.

Nonetheless, we cannot guarantee that the stressful situation that families had to face in the years after the children’s birth did not contribute to increasing parental stress and even affected child at-risk situations. The parental distress has been evaluated with the PSI-SF, one of the instruments commonly used as a diagnostic or screening measure to assess the parenting system and possibly identify at-risk or problematic areas in parental behavior. In the present study, parents were asked to fill it in as a self-report questionnaire that the FPs then collected. This tool per se cannot constitute the basis for a clinical diagnosis. Still, those who emerged as potentially at risk could be advised to pursue a specific clinical assessment (which cannot be done in the context of well-child pediatric visits).

An important consideration is that even though referral to a specialist when needed is foreseen in clinical practice, only 38% of the children with warning signs have been evaluated by a child psychiatrist or a psychologist. In some cases, a diagnostic process might still be ongoing. Thus, the number of children with clinical diagnoses reported in the present study may be underestimated. It is possible that FPs decided to refer only children with a suspected developmental disorder and less severe warning signs required only a follow-up by the FPs. Lastly, in Italy, mothers are the caregivers who more frequently bring their children to the well-child visits; reduced paternal involvement in the present study confirmed this assumption. Greater paternal involvement in monitoring a child’s development should be encouraged. Therefore, it will be necessary to monitor the development of this cohort in future years to confirm the accuracy of the proposed assessment model.

This study demonstrated the feasibility of a new approach: combining the results of parental perspective and pediatrician’s evaluation could help identify children at risk of neurodevelopmental disorders early. Thus, the present study does lay the foundation for future studies on early screening during well-child visits. Moreover, its longitudinal design permits overcoming the large variability of the developmental trajectory at early stages: children should be followed up in terms of development at different time points regardless of screening status; repeated developmental assessments over time are more informative than one-time assessments in planning investigations and management. Pediatricians should also consider parental emotions, especially depression, and stress, which, as demonstrated, could be evaluated with self-report questionnaires and could have a potential association with children’s outcomes.

Hopefully, this study will help bridge the gap between screening tools and a practical protocol that can be applied in the FP’s setting, enhancing the capability for early identification of children who appear to be at low risk of a developmental disorder. Further scientific studies with more sophisticated designs are needed to better understand the different aspects of possible developmental disorders and associated factors; moreover, future research is required to ensure that developmental interventions are effectively conducted on children at risk and referred to specialists. An ongoing relationship between pediatricians and parents will guarantee better neurodevelopmental outcomes.

The present study demonstrated the feasibility and usefulness of child assessment that integrates the FPs’ and parents’ perspectives and evaluations: future studies might implement a similar approach, asking parents to fill in different questionnaires (as the MCHAT used here) to report on their child’s development. Secondly, while the agreement between parents and FPs was only minimum, the combined sensitivity was higher. Thus, monitoring the infant’s development in different contexts is crucial and should always be recommended. Future directions should follow up with children and parents at later stages, possibly involving other figures with a primary role in children’s development, such as educators and teachers. Finally, this study highlights variables that could significantly impact both child development and parental distress. Valuable practical interventions designed around these factors could be implemented and used by the FPs to support parents. Where significant stress is observed, parents might benefit from information on positive behaviors (i.e., supportive parental actions) to lower perceived stress and support a child’s development. Where this is not enough, FPs can recommend clinical follow-ups.