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. Author manuscript; available in PMC: 2022 Apr 1.
Published in final edited form as: Child Neuropsychol. 2020 Dec 21;27(3):351–370. doi: 10.1080/09297049.2020.1861229

Social-environmental moderators of neurodevelopmental outcomes in youth born preterm: A systematic review

Sarah E Bills a, Julia D Johnston a, Dexin Shi a, Jessica Bradshaw a
PMCID: PMC7969400  NIHMSID: NIHMS1657698  PMID: 33342364

Abstract

Objective:

Preterm birth represents a significant medical event that places infants at a markedly greater risk for neurodevelopmental problems and delays. Although the impact of medical factors on neurodevelopment for those born preterm has been thoroughly explored, less is known about how social-environmental factors (e.g., socioeconomic status, family functioning) moderate outcomes. This review explores the quantity and methodological rigor of research on social-environmental factors as moderators of the relationship between preterm birth and neurodevelopmental outcomes.

Methods:

Articles published between January 1980 and December 2016 were identified from a comprehensive meta-analysis and systematic review on neurodevelopmental outcomes following preterm birth (Allotey et al., 2018). A systematic review of MEDLINE was conducted to identify articles published from January 2017 through April 2019.

Results:

Eighty articles met the inclusion criteria. The majority of studies matched preterm and control groups on social-environmental factors (n=49). The remaining studies included social-environmental factors as moderators (n=13) or correlates (n=11) of neurodevelopmental outcomes. Only seven studies did not include reports on social-environmental factors.

Conclusions:

This systematic review suggests that social-environmental factors are often considered to be ancillary risk factors to the larger medical risk imparted by prematurity. Studies typically focused on socioeconomic status rather than more modifiable parent/family factors that can be targeted through intervention (e.g., parental mental health) and evidenced mixed findings regarding the significance of social-environmental factors as moderators. Further research is needed to identify the relative influence of social-environmental factors to inform future psychosocial interventions.

Keywords: preterm, neurodevelopmental outcomes, socioeconomic status, parent and family functioning, cognitive functioning

Recent medical advances have significantly improved survival rates of infants born premature (<37 weeks). However, these decreased mortality rates have been accompanied by an increased acknowledgment of related neurodevelopmental impairments and delays. Research has identified preterm birth as a risk factor for deficits in general intellectual functioning and specific cognitive domains (e.g., executive functioning, attention), as well as behavioral, and academic functioning (Aarnoudse-Moens et al., 2009; Allotey et al., 2018; Arpi & Ferrari, 2013; Böhm et al., 2004; Breeman et al., 2016; Lundequist et al., 2012). These deficits often persist from infancy through adulthood (Baron & Rey-Casserly, 2010; Breeman et al., 2015).

The increased risk of adverse outcomes highlights the importance of identifying risk factors for poor outcomes in the preterm population. The impact of medical factors, namely degree of prematurity, on cognitive, behavioral, and academic functioning has been well studied (Aylward, 2014). In a recent systematic review and meta-analysis on the association between preterm birth and neurodevelopmental outcomes by Allotey and colleagues (2018), extremely low gestational age at birth (i.e., < 28 weeks) was associated with the highest risk of impairment; however, children born very and moderately preterm (i.e., 28–34 weeks) evidenced nearly the same levels of deficits in performance as children born extremely preterm. The review notes there are areas of investigation where research is lacking, namely, consideration of risk factors beyond prematurity. Given that behavioral-level outcomes such as cognitive and academic performance are best conceptualized as biopsychosocial phenomena with multiple influences, it is important to consider the influence of other social and environmental risk factors (Maggi et al., 2010; Santos et al., 2008; Black & Hoeft, 2015).

Social-environmental factors are a particularly salient category of risk and protective factors that encompass both proximal and distal social influences. Social-environmental factors include relatively static indices of socioeconomic status (SES), such as parental income and education level, as well as more modifiable characteristics related to family functioning, such as family mental health, parenting knowledge/experience, and parent-child interactions. Increased social-environmental risk (e.g., low income/maternal education, single parent household, low maternal social support) is known to increase risk for adverse health and neurodevelopmental outcomes among children and adolescents in the general population (McEwen & Gianaros, 2010; Ruiz et al., 2016). Although more traditional measures of social-environmental risk, such as SES, are more readily measurable, there are benefits to including modifiable measures of social-environmental risk. Interventions that target social-environmental factors such as parent and family functioning have been found to improve early neurodevelopmental outcomes within preterm populations, highlighting the salience of these more modifiable factors (Melnyk et al., 2001; Nordhov et al., 2010). Additionally, within medically vulnerable populations, research indicates there is an additive relationship among social-environmental and medical factors, wherein children with health concerns often experience the double burden of medical and social-environmental risk factors (Laucht et al., 1997).

Although increased social-environmental risk is known to be a precipitating factor for the occurrence of premature birth, less is known about its impact following birth (Kramer et al., 2001; Thompson et al., 2006). To the authors’ knowledge, only one systematic review has explicity focused on the relationship between neurodevelopmental outcomes and social-environmental factors for children born preterm (Wong & Edwards, 2013). Across studies, this review found that socioeconomic disadvantage was significantly associated with poorer cognitive outcomes. However, as the focus of the review was the effect of SES on cognitive outcomes in preterm infants, several issues were not discussed, including: the frequency with which studies include SES as a factor associated with cognitive outcomes, the impact of SES on behavioral and academic outcomes, and the impact of more modifiable social-environmental factors on cognitive outcomes. Lastly, the review did not discuss moderation studies that explore the interaction between medical factors, such as prematurity, and social-environmental factors (Wong & Edwards, 2013). Although examining associations between social-environmental factors and outcomes is an important step in identifying pertinent risk factors, moderation analyses are needed to understand how social-environmental risk may manifest differently for preterm children compared to full-term children. In addition, the identification of significant moderating variables can be useful in guiding the allocation of resources as they delineate the subgroups of children and families at greatest need for prevention and intervention efforts. As such, there is a need for further investigation to quantify and clarify the role of social-environmental factors in the neurodevelopment of preterm children and adolescents (Baron & Rey-Casserly, 2010).

The purpose of the current review is to address these gaps in the literature by investigating the quantity and methodological rigor of research on social-environmental moderators of poor neurodevelopmental outcomes among children born preterm. First, the current review will determine how frequently social-environmental moderators are included in research studies that examine the relationship between preterm birth and neurodevelopmental outcomes. This first aim will provide broad information on the quantity of research on social-environmental moderators over the past four decades as well as summarize the relationship between these social-environmental factors and neurodevelopmental outcomes. Second, the current review will evaluate the methodological rigor of studies that included social-environmental moderators by examining general study characteristics that are indicative of study quality, such as design features, as well as study characteristics specific to moderation analyses. Moderators of interest include social-environmental risk and protective factors, with particular attention paid to potentially modifiable factors in an effort to identify areas for future intervention efforts. Neurodevelopmental outcomes of interest include cognitive, motor, behavioral, and academic functioning.

Methods

The methods adopted for this systematic review were based on those outlined in the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines (Moher et al., 2009).

Eligibility Criteria for Study Inclusion

Studies published between January 1980 and April 2019 that reported on neurodevelopmental outcomes (e.g., cognitive, motor, academic, and behavioral) of children born before 34 completed weeks of gestation were included in the current review. Studies were excluded if they solely reported outcomes for young adults (i.e., 18+) or children less than two years of age, as the current review is focused on functioning in childhood and adolescence. Interventional studies, abstracts, reviews, and case reports/series were excluded. Consistent with guidelines from the American Academy of Pediatrics which recommends the use of corrected age until two years of age, studies that used corrected age past two years of age were excluded (American Academy of Pediatrics, 2004; Bernbaum et al., 2009). Studies were excluded if their primary focus was the association between neurodevelopmental outcomes and structural and functional brain changes. Finally, studies were excluded if the full text was not available in English. This increases risk for a degree of bias in the final sample of included studies, but was judged an acceptable risk by the authors.

Data Sources and Search Strategies

Studies published between January 1980 and December 2016 were identified by the primary author (S.E.B.) from the comprehensive meta-analysis and systematic review conducted by Allotey and colleagues (2018). The references identified from Allotey and colleagues were accessed through the online supplemental resources. An electronic database search of MEDLINE via the OVID platform was conducted to identify additional articles published between January 2017 through April 2019. Search terms were designed to capture all studies that included neurodevelopmental outcomes of preterm infants and followed those used by Allotey and colleagues. Search terms included ‘preterm’, ‘premature’, or ‘prematurity’ paired with outcome terms of ‘child development,’ ‘developmental disabilities’, ‘neurodevelopment’, ‘learning disorders’, ‘mental disorders’, ‘psychomotor disorders’, ‘language development’, and ‘adverse outcomes’, among others. Search terms related to social-environmental factors or moderation analyses were not included as the search was designd to identify studies regardless of the inclusion of such factors. For a complete list of search terms, see Appendix A.

Study Selection

Study selection occurred in two phases. First, the primary author (S.E.B.) reviewed 74 studies initially identified in the reference section of the article by Allotey and colleagues (2018). Of the original 74 articles, 16 were excluded as they included samples outside of the gestational age range (i.e., > 34 weeks). Of the 58 remaining studies, one was excluded as the full text was not available in English, one was excluded due to the use of corrected age for children older than age two, and four studies were excluded as their outcomes fell outside the targeted age range of the current review, yielding a total of 52 studies. In the second phase, an electronic database search was conducted to identify articles published between January 2017 and April 2019, which yielded 5634 articles (see Figure 1). The procedures for identifying papers through electronic databases followed the search strategy utilized by Allotey and colleagues. Two independent reviewers conducted a title review and identified 200 eligible studies for further abstract review. Of these 200 articles, 36 were included for a full article review (Kappa = .88) and 28 articles ultimately met final inclusion criteria (Kappa = .72) (see Figure 1). Any disagreement between reviewers was resolved through discussion. Thus, study selection yielded a total of 80 studies included in the current review. Selected articles were then examined to determine how each study collected and incorporated social-environmental factors into their analyses. Summary measures were descriptive in nature and included the frequency of inclusion of social-environmental factors in analyses as well as the frequency of inclusion of specific categories of social-environmental factors.

Figure 1.

Figure 1.

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Flow diagram of systematic literature search for articles from published between January 1980 and April 2019. Numbers in brackets denote articles identified from the comprehensive meta-analysis and systematic review conducted by Allotey and colleagues.

Design and Reporting Index

All studies that included moderation analyses were assessed for key features using a design and reporting index (see Appendix B). In line with other systematic reviews interested in assessing general study characteristics (Frazier et al., 2017), the index consisted of variables related to study design and methologoical rigor to both facilitate the assessment of possible risk of bias and provide information on consistency of reporting across studies. Established indicies of study and reporting quality (e.g., the Quality in Prognosis Studies) were referenced and informed the present study’s checklist (Hayden et al., 2013). Specifically, items from the Quality in Prognosis Studies were modified and additional items were developed by authors (S.E.B. & J.D.J.), ultimately resulting in the inclusion of 11 items. Of note, some items are not standard measures of study quality, but instead reflect key features pertinent to the research questions of our review. The 11 items included in the checklist fell into three broad categories: A) sampling and participants (e.g., did studies include recruitment methods for both preterm and control groups?), B) measurement of social-environmental factors (e.g., were multiple indicators of SES used to generate a composite score?), and C) statistical methods (e.g., did authors use rigorous methods to control for environmental influences?). Articles were reviewed by two independent reviewers and variables were coded from available study characteristics as either yes(✓)/not reported(-) or yes (✓)/partial (P)/not reported(-).

Results

A review of the methodology and outcomes of the 80 studies revealed four primary ways in which social-environmental factors were considered: Studies that reported on social-environmental factors as moderators of neurodevelopmental outcomes (Category 1), studies that reported on any associations (e.g., regression or correlation analyses) between social-environmental factors and neurodevelopmental outcomes (Category 2), studies that matched preterm and control groups on social-environmental factors or treated social-environmental factors as covariates (Category 3) and studies that included no reports on social-environmental factors (Category 4).

Category 1 included 13 of the total 80 studies (16%) and reported analyses with social-environmental variables as moderators of cognitive, behavioral, and academic outcomes (see Table 2). The most common social-environmental factors included were measures of SES, namely maternal education; however, four of the studies included measures of parent and family functioning (e.g., parental stress, family environment, parenting practices) in addition to indices of SES (Lean et al., 2018; Levy-Shiff et al., 1994; Sommerfelt et al., 1995; Teplin et al., 1991). All four of these studies used parent self-report questionnaires completed by the mother. A variety of different questionnaires were used, which included both multidimensional (e.g., Family Assessment Device, Parenting Stress Index) and unidimensional measures (e.g., Index of Parental Attitudes, Burnout Measure) of parent and family functioning. All studies that included modifiable parent and family measures examined risk factors, with no mention of protective or resilience factors. An examination of general study characteristics of Category 1 studies indicated no systematic variability in the inclusion of modifiable social-environmental variables based on sample size, country of origin, or age of sample. However, it is notable that three of the four studies that included the more modifiable measures of social-environmental factors were published between 1990 and 2000. There were no Category 1 studies published in the 1980s, suggesting minimal interest in social-environmental factors as moderators before the 1990s.

Table 2.

Descriptive information, social-environmental factors, and neurodevelopmental outcomes for articles that reported on any associations between social-environmental factors and neurodevelopmental outcomes

Study Population
Study GA (weeks) BW (g) Age Sample Size Neurodevelopmental outcome(s) Social-environmental factor(s) examined Significant association reported?
Botting et al. (1997) <30 <1501 12yo N=284 Cognitive abilities, academic achievement & behavioral difficulties SES Yes
Saavalainen et al. (2008) <32 M=1456.8 9yo, 16yo N=81 Cognitive abilities & academic achievement SES Yes
Saigal et al. (2000) M=27 <1000 12yo–16yo N=274 Cognitive abilities & academic achievement SES Yes
Borchers et al. (2019) <32 M=1282 6yo, 8yo N=89 Cognitive abilities SES Yes
Broring et al. (2018) <32 <2065 8yo–9yo N=114 Cognitive abilities & behavioral difficulties SES Yes
O’Meagher et al. (2017) <33 Not reported 4yo–5yo N=218 Cognitive abilities & behavioral difficulties SES Yes
Danks et al. (2017) M=27 <1000 11yo–13yo N=103 Behavioral difficulties & motor skills SES No
Litt et al. (1995) M=31 <1501 1yo, 2yo, 6yo N=39 Cognitive abilities & motor skills SES Yes
Luu et al. (2011) M=28 <1250 16yo N=439 Cognitive abilities SES Yes
Bohm et al. (2002) <27 <1500 5yo Cognitive abilities SES Yes
Schneider et al. (2014) ≤32 Not reported 10yo–14yo N=145 Cognitive abilities SES Yes
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Note.

BW=Birthweight; GA= Gestational age; SES=Socioeconomic status

A summary of findings from the design and reporting index for the Category 1 studies can be found in Table 3. Forty-six percent of studies met or partially met nine or more of the 11 total criteria and 85% of studies met or partially met seven or more of the 11 criteria, indicating consistency across studies and a generally low risk of bias based on methodological factors. Less than 40% of studies met or partially met the following criteria: Medical/health comorbidities excluded for control group; parent and family functioning variables included in addition to SES; and use of rigorous methods to control for environmental influences (i.e., sibling or classroom control). Also of note, only seven of the 13 studies in Category 1 included indicators that moderation analyses were pre-planned as evidenced by references to moderation analyses in the study hypotheses. As analyses of social-environmental factors were not necessarily a primary aim for many of the studies, there is a relatively low risk for the systematic exclusion of studies with null findings.

Table 3.

Design and reporting index ratings for articles that reported on social-environmental factors as moderators of neurodevelopmental outcomes.

Study 1. 2. 3. 4. 5. 6. 7. 8. 9. 10. 11.
Kilbride et al. (2004) ✓ ✓ ✓ ✓ P ✓ ✓ - ✓ - ✓
Scott et al. (2012) ✓ ✓ ✓ - ✓ ✓ ✓ - ✓ - ✓
Beauregard et al. (2018) ✓ ✓ ✓ ✓ ✓ P ✓ - - ✓ ✓
Lean et al. (2018) ✓ P ✓ ✓ P ✓ ✓ ✓ - ✓ ✓
Linsell et al. (2018) ✓ ✓ - - P ✓ - - ✓ ✓ ✓
Taylor et al. (2018) ✓ ✓ ✓ - ✓ ✓ ✓ - ✓ - -
Levy-Shiff et al. (1994) P P ✓ ✓ P ✓ ✓ ✓ - ✓ -
Ross et al. (1990) ✓ P ✓ - P ✓ ✓ ✓ - ✓ ✓
Saigal et al. (1991) ✓ P ✓ - ✓ ✓ ✓ - - ✓ ✓
Sommerfelt et al. (1995) ✓ ✓ ✓ ✓ P ✓ ✓ ✓ - ✓ ✓
Taylor et al. (2000) ✓ P ✓ - ✓ ✓ ✓ - ✓ - ✓
Teplin et al. (1991) ✓ P - - P ✓ - ✓ - - ✓
Wolke & Meyer (1999) ✓ ✓ - - P ✓ ✓ - - - -
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Key: (✓)=reported, (P)=partially reported, (-)= did not report

1. Methods to identify the sample, place of recruitment, and period of recruitment reported for preterm group?

2. Methods to identify the sample, place of recruitment, and period of recruitment reported for control group?

3. Medical/health comorbidities excluded from preterm group?

4. Medical/health comorbidities excluded from control group?

5. Age at testing, gender, and race/ethnicity reported for all participants?

6. Gestational age and birthweight reported for preterm group?

7. Composite/multiple indicators of socioeconomic used in analyses?

8. Parent and family functioning variables included in addition to SES?

9. Use of rigorous methods to control for environmental influences (i.e., sibling or classroom control)?

10. Evidence that moderation analyses were pre-planned (e.g., noted in hypotheses)?

11. Description of moderating analyses in both statistical analysis and results sections?

Four of the 13 studies in Category 1 found social-environmental factors to be significant moderators of the relationship between prematurity and neurodevelopmental outcomes (Lean et al., 2018; Levy-Shiff et al., 1994; Teplin et al., 1991; Ross et al., 1990). Specifically, increased social-environmental risk had a more negative impact on measures of general intelligence, attention, and behavioral functioning in the preterm group compared to full-term infants. However, the precise role and type of the social-environmental factors differed across studies. One study solely used SES as a measure of social-environmental risk and found that premature children with lower SES backgrounds, but not full-term children, evidenced poorer behavioral outcomes than children with higher SES backgrounds (Ross et al., 1990). The remaining three studies included both SES and parent and family factors in moderation analyses (Lean et al., 2018; Levy-Shiff et al., 1994; Teplin et al., 1991). Levy-Shiff and colleagues (1994) found parent and family factors, namely parental involvement, to be as influential as traditional measures of SES. In contrast, Teplin and colleagues (1991) and Lean and colleagues (2018) identified only measures of SES as significant moderators. However, of interest, Lean and colleagues found that SES and parent and family factors (i.e., parenting stress) exerted independent influences on cognitive and language outcomes, suggesting parent and family factors offer predictive value above and beyond SES alone. In the nine remaining studies with nonsignificant moderation findings, elevated social-environmental risk was still predictive of poorer outcomes.

Sommerfelt and colleagues (1995) was the only study from Category 1 with nonsignificant moderating effects that included more modifiable measures of parent and family functioning. As such, a post hoc power analysis was conducted to determine if the study was adequately powered to detect significant moderating effects. A benchmark effect size of f2= .009 was used given a systematic review showing .009 to be the average effect size in tests of moderation (Aguinis et al., 2005). Using this benchmark, the post hoc power estimate for the study by Sommerfelt and colleagues was .33, indicating a two-thirds likelihood of failing to detect a significant moderating effect.

Eleven studies (14%) fell within Category 2 and reported associations between at least one social-environmental factor and neurodevelopmental outcome variable (see Table 1). These included both correlational and regression analyses. All studies used indices of SES as their measure of social-environmental risk and all but one of the 12 studies reported that lower SES was either predictive of or associated with poorer performance on a variety of neurodevelopmental measures, including cognitive, academic, and behavioral outcomes. A recurring theme discussed by the authors of these studies was the detrimental impact of the aggregation of medical and social-environmental risk factors.

Table 1.

Descriptive information, social-environmental factors, and neurodevelopmental outcomes for articles that reported on social-environmental factors as moderators of neurodevelopmental outcomes.

Study Population

Study		 GA (weeks) BW (g) Age Country Sample Size Neurodevelopmental outcome(s) Social-environmental factor(s) examined Significant moderating
effect reported?
Kilbride et al. (2004) M=26 <801 3yo–5yo United States N=50 Cognitive abilities & motor skills SES No
Scott et al. (2012) <28 <1000 Kindergarten (M= 5.96yo) United States N=259 Cognitive abilities, academic achievement & behavioral difficulties SES No
Beauregard et al. (2018) <27, ≤28–33 Not reported 2yo & Kindergarten (M= 5.69yo) United States N=3800 Cognitive abilities & academic achievement SES No
Lean et al. (2018) <30 M=943.14 2yo & 5yo United States N=146 Cognitive abilities & academic achievement Social risk*, parenting stress, parent child interactions, family functioning Yes
Linsell et al. (2018) <26 Not reported 6yo, 11yo, 16yo United Kingdom N=475 Cognitive abilities & motor skills SES No
Taylor et al. (2018) <28 <1000 Kindergarten (M=5.94yo), first grade (M=6.96yo) & second grade (M =8.00yo) United States N=256 Cognitive abilities & academic achievement SES No
Levy-Shiff et al. (1994) <35 <1500 6yo–7yo, 13yo–14yo Israel N= 180 Cognitive abilities & behavioral difficulties SES*, family environment, parent-child relations*, parental stress Yes
Ross et al. (1990) M=29.3 <1501 7yo–8yo United States N=687a Behavioral difficulties SES* Yes
Saigal et al. (1991) M=27 <1000 7.5yo–8yo Canada N=258 Cognitive abilities, academic achievement & motor skills SES No
Sommerfelt et al. (1995) Not reported <2000 5yo Norway N=307 Cognitive abilities SES, maternal social support, psychological distress, childrearing attitudes No
Taylor et al. (2000) M=25.7
M=29.4		 <750, <1500− 750 Early school age (M=6.7yo), Middle school age (M=11.0yo) United States N=164 Cognitive abilities, academic achievement & behavioral difficulties Sociodemographic risk No
Teplin et al. (1991) <31 <1001 6yo United States N=54 Cognitive abilities & behavioral difficulties SES*, maternal stress Yes
Wolke & Meyer (1999) <32 <1330 6.25yo Germany N=528a Cognitive abilities & academic achievement SES No
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Note.

*

Denotes the significant moderating variable(s) for studies with significant findings

a

Sample size includes a normative comparison group

BW=Birthweight; GA= Gestational age; SES=Socioeconomic status

The 49 studies (61%) in Category 3 treated social-environmental factors as nuisance variables, reporting social-environmental factors either as part of their matching procedure between full-term and preterm groups or including them as covariates in their primary analyses (see Appendix C for full list of references). In line with findings from the previous two categories, the most commonly reported social-environmental variables within this category were measures of SES such as maternal education and income. Lastly, seven studies (9%) fell within Category 4 and included no mention of social-environmental factors in their methodology or data analysis sections (Celik et al., 2018; Foulder-Hughes & Cooke, 2003; Hirvonen et al., 2017; Johnson et al., 2010; Majewska et al., 2018; Sajaniemi et al., 1998; Van Braeckel et al., 2010).

Discussion

Neurodevelopmental deficits in the areas of cognitive, behavioral, and academic functioning are a common concern throughout development in children born preterm. This review explored the inclusion of social-environmental factors in research on neurodevelopmental outcomes among children born preterm, with the primary aim of investigating the quantity and methodological rigor of research on social-environmental moderators of neurodevelopmental outcomes. Cognitive, behavioral, and academic outcomes are typically conceptualized as biopsychosocial phenomena, yet it appears that the predominant research methodology used to date has focused on isolating the impact of biomedical factors without integrating potential social-environmental moderators. A review of the current literature indicated that the vast majority of studies that included social-environmental factors fell in Category 3 (matching/covariate studies), followed by Category 2 (association studies), and, lastly, Category 1 (moderation studies). Findings will be discussed in this order.

The preponderance of studies considered social-environmental factors as covariates or nuisance variables (i.e., Category 3), implying that social-environmental variables are most frequently conceptualized as ancillary factors to the medical risk imparted by prematurity. Few studies included analyses on or reported any direct association between social-environmental factors in relation to neurodevelopmental outcomes (i.e., Category 2). Overall, results from these studies identified increased social-environmental risk, namely low SES, as a salient contributing factor to impairments in functioning across cognitive, behavioral, and academic outcomes. Such findings on the association between social-environmental factors and outcomes are aligned with research on the detrimental impacts of increased social and environmental risk in preterm children (McEwan & Gianaros, 2010; Ruiz et al., 2016).

Although research from the previously discussed category of studies (i.e., Category 2) was limited, even fewer studies have included moderation analyses to identify the risk and protective role that such social and environmental factors may have in moderating the effects of prematurity on neurodevelopmental outcome. Studies that included moderation analyses (i.e., Category 1) encompassed a range of cognitive, behavioral, and academic outcomes. Results from the design and reporting quality index, which summarized study characteristics related to study design and methodology, indicate that the majority of studies included pertinent information on sampling and recruitment procedures, statistical methods, and the measurement of social-environmental factors. This suggests that, overall, there are no significant concerns relating to design and methodological factors that affect the interpretation of study findings and indicates reasonably high consistency across studies. However, it is notable that only approximately half of the studies reported pre-planned moderation analyses, which suggests that analyses examining moderating effects of social-environmental factors may not have been the primary focus of many of the studies.

There were mixed findings regarding the relative importance of social-environmental variables, with roughly one-third of the studies finding significant moderating effects. SES was the most common indicator of social-environmental risk and was included in all of the moderation studies. Overall, findings indicate that in the context of the biological risk factor of preterm birth, social-environmental risk may place children at an even greater likelihood for poor outcomes. Of note, however, three of the four studies that found significant moderating effects included more modifiable measures of parent and family functioning, such as parenting stress and parent-child interactions, as indicators of social-environmental risk. This suggests that the inclusion of more targeted and modifiable factors may increase the likelihood of identifying significant moderating effects. Furthermore, post hoc power analyses for the one study that included measures of parent and family functioning with nonsignificant moderating findings revealed that the study was considerably underpowered to detect moderation effects. As such, difficulties achieving adequate power to detect moderating effects may be responsible in part for the mixed findings on the moderating effects of social-environmental factors and may contribute to the overall paucity of literature on moderating effects of social-environmental factors on neurodevelopmental outcomes in the preterm population.

Although the inclusion of more modifiable measures of social-environmental factors may influence the identification of moderating effects, studies with significant moderation findings reached differing conclusions regarding the relative importance of various categories of social-environmental factors. Of the three studies that included both SES and more modifiable risk factors, one study found both SES and parent and family functioning to be significant moderators, one study identified solely parent and family functioning as significant moderators, and the final study identified solely SES as a significant moderator. Although there is evidence to suggest that parent and family factors offer predictive value above and beyond SES alone, the limited number of studies and these mixed findings highlight an inadequate understanding of the role of different indicators of social-environmental risk as well as the lack of consensus on the impact of social-environmental risk in preterm children.

There are a number of methodological factors that may contribute to these mixed findings. First, social-environmental risk is both multidimensional and complex and, as such, is difficult to capture with the broad variables typically used as proxies for SES. Therefore, the use of broad measures, such as maternal education, as proxies for SES may limit their ability to detect more subtle moderating effects. Second, measures of SES such as income and education level are generally static, making it difficult to pinpoint underlying mechanisms which are an important component of translating findings into interventions. As such, there are distinct advantages conferred by including more modifiable and targeted social-environmental characteristics, such as family dynamics, parenting, and parent-child interactions. Indeed, early interventions that target parent and family functioning of preterm infants have shown moderate success in improving neurodevelopmental outcomes (Spittle, 2017). However, there is less research on interventions conducted during the developmental periods of childhood and adolescence, indicating a need for future research to identify pertinent modifiable social-environmental factors and examine the relative influence of such factors across development to better inform future intervention efforts. Furthermore, it is important to consider the ways in which culture influences the relationship between modifiable social-environmental factors and developmental outcomes. The relative importance of parent and family factors and expectations for development in youth varies across cultural groups due to differences in social practices and norms (Bornstein, 2012; Lansford et al., 2018). Although cross-cultural comparisons of social-environmental factors are outside the scope of the current review, it is important to consider such factors when interpreting results and developing interventions.

The publication dates of the studies that included social-environmental factors are also notable, with more than half of the studies published at or before the year 2000. Given the acknowledgement in previously discussed research of the important role of social and environmental factors, the lack of recent studies including social factors suggests little attention is being paid to biopsychosocial integration as a scientific framework. As the survival rates of children born preterm continue to increase due to medical advancements, it will become more important to acknowledge and discern the differential impact of social-environmental risk on preterm populations. The impact of such medical advancements and subsequent changes in care guidelines can have differential impacts on children and families, as neonatal and obstetric care frequently differ based on regions, institutions, and characteristics of the patient population served such as socioeconomic status (Grobman et al., 2014; Van Reempts et al., 2007). The impact of these systems-level factors will be important to consider when examining the association of specific risk factors with particular cognitive, behavioral, and academic outcomes. Ultimately, this can inform efforts to tailor future intervention efforts to the unique set of risk factors associated with preterm birth.

It is also important to consider the types of neurodevelopmental outcomes included within moderation studies. Cognitive functioning was the most frequent outcome of interest, followed by academic functioning, behavioral difficulties, and motor skills. The current review intentionally included a broad range of neurodevelopmental outcomes given the limited number of moderation studies; however, it is important to consider the differential impact of social-environmental factors on specific neurodevelopmental outcomes. A majority of studies have demonstrated that social-environmental factors confer broad risk for cognitive and motor impairment (Johnson et al., 2015; Koutra et al., 2011; Msall et al., 1998; Wickremasinghe et al., 2011). Limited literature suggests cognitive outcomes, rather than motor skills, are most sensitive to factors like maternal education and socioeconomic disadvantage (Koutra et al., 2011; Vanderveen et al., 2009). As such, it will be important for future research to explore the effects of social-environmental influences on specific neurodevelopmental outcomes.

The majority of articles included in this review reported birthweight in addition to gestational age. Although there is a significantly higher incidence of low birthweight among preterm births when compared to full term births, the two do not always overlap. Currently, there is a lack of consensus on the relative contribution of both risk factors on neurodevelopment. This is apparent in the literature on small for gestational age (SGA) children, which suggests neurodevelopmental impairments are present among term SGA children but are greater among preterm SGA children (de Bie et al., 2010; Savchev et al., 2013). Although differentiating the impact of gestational age and birthweight was outside the scope of this review, additional research is needed to better understand the shared and unique mechanisms through which these risk factors impact development.

Limitations

There were a number of limitations of the current review. First, as studies with samples in the late preterm range (34–37 weeks gestation) were excluded, our results may not be reflective of research on social-environmental factors in late preterm populations. However, given the different degree of medical risk conferred by late preterm populations, the authors believe that the benefits of focusing on a narrower range of prematurity was warranted. Second, some outcomes associated with preterm birth, such as autism spectrum disorder, fell outside the scope of this review but should be studied in future research. Third, although the largely qualitative approach of the current review was needed to provide an initial assessment of the frequency of inclusion of social-environmental factors as moderators in this field of research, it will be important for future research to examine this in a more quantitative nature through the use of meta-analytic data analyses. Fourth, the adherence to American Academy of Pediatrics guidelines for corrected age may have resulted in the exclusion of more recent studies that used corrected age for older children. As such, there is a need for future reviews to examine the inclusion of social-environmental factors in studies using corrected age. Lastly, this review does not address the possibility that social-environmental factors themselves can serve as a risk factor for preterm birth.

Conclusion

The results from this review provide insight into the field’s current conceptualization of the importance of social and environmental factors in determining cognitive, behavioral, and academic functioning in preterm children. Findings suggest that there is a need for an expanded investigation on the role of such factors in preterm populations, with a specific focus on the interaction between prematurity and indicators of social-environmental risk such as SES and family functioning. Ultimately, a better understanding of this interplay between medical and social-environmental risk can inform efforts to identify, monitor, and support children who are most vulnerable to adverse neurodevelopmental outcomes.

Funding Statement:

This publication was supported in part by the National Institutes of Health through the following grants: T32-GM081740 (Bills), K23MH120476 (Bradshaw), R21DC017252 (Bradshaw). Its contents are solely the responsibility of the authors and do not necessarily represent the official views of the NIGMS or NIH.

Appendix A.

Search strategy modeled after Allotey and colleagues (2018) used in review. Additional criteria (31–36) added by primary author (S.E.B.).

1. preterm or pre-term or pre term or premature or near-term or prematurity.mp
2. birth or infant or delivery or baby or babies.mp
3. 1 and 2
4. child development.mp
5. developmental disabilities.mp
6. neurodevelopment.mp
7. learning disorders.mp
8. visual perception.mp
9. attention deficit disorder.mp
10. ADHD.mp
11. mental disorder.mp
12. intellectual disability.mp
13. psychomotor disorders.mp
14. psychomotor performance.mp
15. speech disorder.mp
16. language disorder.mp
17. language development.mp
18. language development disorder.mp
19. motor skills disorder.mp
20. movement disorder.mp
21. cognitive or cognition or neuromotor or locomotor or psychomotor or intelligence or neurobehavioural or neurobehavioral.mp
22. neurodevelopment or neural development.mp
23. follow up.mp
24. adverse outcome.mp
25. long-term outcome or long term outcome or outcome.mp
26. 4 or 5 or 6 or 7 or 8 or 9 or 10 or 11 or 12 or 13 or 14 or 15 or 16 or 17 or 18 or 19 or 20 or 21 or 22
27. 23 or 24 or 25
28. 3 and 26 and 27
29. limit 28 to yr=“2017 -Current”
30. review.pt.
31. 29 not 30
32. remove duplicates from 31
33. meta-analysis.ti.
34. 32 not 33
35. randomized.ti.
36. 34 not 35
Open in a new tab

Appendix B

Design and Reporting Index

1. Methods to identify the sample, place of recruitment, and period of recruitment reported for preterm group? Yes
Partial
Not reported
2. Methods to identify the sample, place of recruitment, and period of recruitment reported for control group? Yes
Partial
Not reported
3. Medical/health comorbidities excluded from preterm group? Yes
Not reported
4. Medical/health comorbidities excluded from control group? Yes
Not reported
5. Age at testing, gender, and race/ethnicity reported for all participants? Yes
Partial
Not reported
6. Gestational age and birthweight reported for preterm group? Yes
Not reported
7. Composite/multiple indicators of socioeconomic used in analyses? Yes
Not reported
8. Parent and family functioning variables included in addition to SES? Yes
Not reported
9. Use of rigorous methods to control for environmental influences (i.e., sibling or classroom control)? Yes
Not reported
10. Evidence that moderation analyses were pre-planned (e.g., noted in hypotheses)? Yes
Not reported
11. Description of moderating analyses in both statistical analysis and results sections? Yes
Not reported
Open in a new tab

Appendix C

Anderson et al., 2003

Anderson et al., 2010

Arhan et al 2017

Ask et al., 2018

Baron et al., 2012

Bayless & Stevenson, 2007

Bolk, Farooqi, et al., 2018

Bolk, Padilla et al., 2018

Bowen et al., 2002

Breeman et al., 2015

Brósch-Fohraheim, 2019

Brostrom et al., 2018

Censullo, 2014

Fjortoft et al., 2015

Garfield et al., 2017

Giordano et al., 2016

Gray et al., 2006

Guarini et al., 2019

Hallin et al., 2010

Halsey et al.,1996

Johnson et al., 2009

Kelly et al., 2018

Leijon et al., 2018

Linsell et al., 2019

Lundequist et al., 2015

Lundequist et al., 2013

Luoma et al., 1998

Magill-Evans et al., 2002

Marlow et al., 1989

McDonald et al., 1989

Mu et al., 2008

Munck et al., 2010

Munck et al., 2012

Ni et al., 2011

Nyman et al., 2019

Putnick et al., 2017

Rajput et al., 2017

Roberts et al., 2011

Rose et al., 1996

Saigal et al., 2003

Schiariti et al., 2007

Silva et al., 1984

Sommerfelt et al., 1993

Stjernqvist et al., 1999

Taylor et al., 2000

Toome et al., 2013

van Dokkum et al., 2018

Van Lieshout et al., 2018

Woodward et al., 2009

Footnotes

Disclosure statement: No potential conflict of interest.

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