Paths of cognitive and language development in healthy preterm infants

Infant Behavior & Development 44 (2016) 199–207

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Infant Behavior and Development

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Paths of cognitive and language development in healthy preterm infants Chiara Ionio a,∗ , Elisa Riboni b , Emanuela Confalonieri a , Chiara Dallatomasina b , Eleonora Mascheroni a , Andrea Bonanomi c , Maria Grazia Natali Sora b , Monica Falautano b , Antonella Poloniato d , Graziano Barera d , Giancarlo Comi b a b c d

CRIdee, Dipartimento di Psicologia, Università Cattolica, Milano, Italy Dipartimento di Neurologia, Servizio di Psicologia, IRCCS S. Raffaele, Milano, Italy Dipartimento di Scienze Statistiche, Università Cattolica, Milano, Italy Dipartimento Materno-Infantile, UO Neonatologia, IRCCS S. Raffaele, Milano, Italy

a r t i c l e

i n f o

Article history: Received 22 December 2015 Received in revised form 13 May 2016 Accepted 8 July 2016 Available online 21 July 2016 Keywords: Prematurity Cognitive development Language development Corrected age Chronological age Age correction for prematurity

a b s t r a c t Objective: Despite the presence of many studies on difficulties related to premature birth, findings on developmental outcomes are heterogeneous. This could be explained from a biological and environmental point of view, but also from a methodological one. The aims of this study were as follows: assess cognitive and linguistic performance using the BSID-III in a population of healthy preterm infants at 24 and 36 months (corrected age); analyze whether the correction for prematurity should be applied, decide when to stop using corrected age and evaluate possible improvements between 24 and 36 months. Methods: Developmental outcome was assessed at 24 and 36 months (corrected age) with the BSID-III in 75 healthy preterm (GA = 32.5 ± 1.97; BW = 1631.55 ± 453.92) and 69 termborn children (GA = 39.77 ± 1.00; BW = 3298.95 ± 457.27). Results: Preterm infants had significantly lower scores than those of term infants in Cognitive (COG) and Language (LANG REC, LANG EC) scales of the BSID-III at both 24 and 36 months, considering both corrected (CA) and chronological (UCA) age. At 24 months, significant differences between corrected and chronological scores were found for each BSID-III scale, while at 36 months, significant differences between corrected and chronological scores were found for LANG scales. Only the scores in the COG scale were statistically different between 24 and 36 months (F = 4.894, P = 0.009, ␩2 = 0.075). Considering only the preterm sample at 24 months, the differences between CA and UCA scores in the COG scale were significantly correlated to GA (p = 0.000) and days in hospital (p = 0.002;), while differences between CA and UCA scores in the LANG ESP scale were significantly correlated to GA (p = 0.010), days in hospital (p = 0.001), and birth weight (p = 0.007). At 36 months, no significant correlations were found.

Abbreviations: NICU, neonatal intensive care unit; BSID-III, Bayley Scales of Infant and Toddler Development; COG, Cognitive score in Bayley Scales of Infant and Toddler Development; LANG RC, Receptive Communication score in Bayley Scales of Infant and Toddler Development; LANG EC, Expressive Communication score in Bayley Scales of Infant and Toddler Development; GA, gestational age; BW, birth weight; CA, corrected age; UCA, chronological age. ∗ Corresponding author. E-mail address: [email protected] (C. Ionio). http://dx.doi.org/10.1016/j.infbeh.2016.07.004 0163-6383/© 2016 Elsevier Inc. All rights reserved.

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Preterm birth is followed by poorer cognitive and language outcomes during infancy than full-term birth. Age correction of prematurity is useful if the child is under 2 years of age; however, our findings raise concerns about the need for age correction, considering that at later ages, healthy preterm children have a higher rate of developmental delay compared with term infants. With regard to cognitive development, preterm children seem to recover from their initial disadvantage; however, with regard to linguistic development, data confirm that preterm infants are at risk for language difficulties. © 2016 Elsevier Inc. All rights reserved.

1. Introduction and objective As the therapy and quality of perinatal care progress, a gradually increasing number of neonates survive preterm birth (Caravale, Mirante, Vagnoni, & Vicari, 2012). Longitudinal follow-up studies have shown that premature birth could be a potential risk factor for the baby (Aarnoudse-Moens, Weisglas-Kuperus, van Goudover, & Oosterlaan, 2009; Arpino et al., 2010). Clinical and experimental evidence supports the negative impact of premature birth on the development of different abilities not only in children born extremely preterm (gestational age (GA) < 28 week), but also in moderate and late preterm (GA ≥ 32 weeks) (Baron, Erickson, Ahronovich, Baker, & Litman, 2011; De Jong, Verhoeven, Lasham, Meijssen, & van Baar, 2015; Nepomnyaschy, Hegyi, Ostfeld, & Reichman, 2012; Sansavini et al., 2011; Voigt et al., 2012). Recent studies have shown how these difficulties during infancy and childhood are linked both with internal factors, which are biologically determined, and external factors of environmental origin (Kerstjens, De Winter, Bocca-T Jeertes, Bos, & Reijneveld, 2012; McMansus & Poehlmann, 2012; Poehlmann et al., 2012; Treyvaud et al., 2011). The risk of morbidity in preterm infants depends on the level of neonatal immaturity in terms of gestational age and birth weight (Saigal and Doyle, 2008). Furthermore, preterm infants are exposed to many environmental stimuli which it is not always possible to study. They don’t experience perinatal rhythmic and kinesthetic stimulations, but they are subject to the acoustic and visual stimuli that characterize the NICU (Negri, 1998; Sansavini & Guarini, 2013). Lastly, the evolutionary paths of preterm births are also determined by factors related to social environment such as difficulties in the early social interactions, characterized by difficulties in the parent-child relationship (Dondi et al., 2008), stress and negative feelings, such as anxiety, depression, guilt and anger experienced by parents (Gray, Edwards, O’Callaghan, & Cuskelly, 2012; Negri, 1998; Rogers, Lenze, & Luby, 2013). The initial biological disadvantages of preterm infants make them more vulnerable, weaker, and less resilient than fullterm children (Aylward, 2009; Dall’Oglio et al., 2010). Different studies show that in preterm infants with no neurological damage, gestational age has an important role for the presence of delays in cognitive and linguistic development especially in the first years of life (Mulder, Pitchford, Hagger, & Marlow, 2009; Sansavini et al., 2011): the difference between preterm infants with no neurological damage and term infants is particularly large for extremely preterm infants (Marlow, Wolke, Bracewell, & Samara, 2005) and it decreases if we consider very preterm (Larroque, Ancel, Marret, Marchand, & André, 2008) and moderate preterm infants (De Jong, Monuteaux, van Elburg, Gillman, & Belfort, 2012). Several studies pointed out the presence of cognitive difficulties in preterm infants’ development during their early years of life, and even thereafter. A longitudinal study conducted on a very large sample of preterm children with no neurological damage showed that 22% of the sample had a cognitive delay (Sansavini & Guarini, 2010). In another study, the cognitive performances of children born very (EG < 32 weeks) and moderately (EG ≥ 32 weeks) preterm were compared to term infants’ performances. The results pointed out that preterm birth could be a risk factor for cognitive development during early childhood, both for children born very preterm and for those born moderately preterm (Voigt et al., 2012). Premature birth could even partially compromise language development (Sansavini et al., 2011; Van Noort-Van der Speck, Franken, & Weisglas-Kuperus, 2012). Most of the studies examined the impact of preterm birth on specific language skills (De Schuymer, De Groote, Beyers, Striano, & Roeyers, 2011; Wolke, Samara, Bracewell, Marlow, & EPICure Study Group, 2008). Only recently, precursors of language, such as receptive and preverbal communication, have been investigated, in order to better understand how these skills are influenced by preterm birth and how their difficult development influences more complex skills in this clinical population (Sansavini & Guarini, 2013). Although the developmental disadvantages of preterm children have been a topic of considerable attention, the results of studies have varied and have led researchers to draw different conclusions about the consequences of preterm birth. Some studies reveal that some preterm children (particularly late-preterm children with no neurological impairment) recover from their initial developmental disadvantages in cognitive and communicative and linguistic domains within their first years of life (Morag et al., 2013; Romeo et al., 2010). However, other studies reveal that preterm children could encounter more new difficulties and disadvantages during their school years than their fullterm peers (Caravale et al., 2012; Dall’Oglio et al., 2010; Johnson et al., 2009; Sansavini & Guarini, 2010). Several studies demonstrated that the development of preschool children with no major neurosensory impairments tends to return to a normal range, although it still remains significantly lower than the one of their term peers (Caravale et al., 2012; Guarini et al., 2009; Gurka, LoCasale-Crouch, & Blackman, 2010). At the same time these studies showed the presence of several difficulties in many neuropsychological functions such as executive functions, visual-spatial skills, short- and long-term

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memory (Aarnoudse-Moens et al., 2009; Mulder et al., 2009). Even their language skills could remain lower than those of children born at term and some of them may develop a language impairment (Van Noort-Van der Speck et al., 2012). These heterogeneous results can be explained both by biological (GA, birth weight) and environmental conditions at birth and, most importantly, by some significant methodological aspects (Sansavini & Guarini, 2010). One of the most problematic methodological aspects is that every preterm newborn displays different clinical conditions, which depend on GA, birth weight (BW), medical condition, NICU features and parental responsiveness. For these reasons, most studies use heterogeneous samples that, added to different evaluation instruments and different follow-up ages, make it difficult to compare the results of different studies (Barre, Morgan, Doyle, & Anderson, 2011; Mulder et al., 2009). Furthermore, in order to better underline the difficulties and developmental delays experienced by this population, it is important to compare the scores of preterm children both with the normative values of the instruments used during follow-up and with the scores achieved by a sample of full-term children (Dall’Oglio et al., 2010). Finally, the most important methodological controversy is whether preterm children’s performance should be assessed using chronological or corrected age. Age correction involves subtracting the number of weeks that the child was born prematurely from the child’s chronological age (UCA) to arrive at the adjusted age (a full-term pregnancy is considered to last 40 weeks). Recommendations for using age correction for the assessment of premature infants can be found in literature as early as 1930 in Mohr and Bartelme, and nowadays, correcting age for prematurity is recommended by the American Academy of Pediatrics (AAP, 2002). For authors who support the use of corrected age (CA) during the assessment of cognitive, language, motor, and social interaction skills, UCA would underestimate developmental progress, and there would be a higher rate of preterm infants reported as suspect, or functioning at a very low-average level, when in fact they are normal, leading to undesirable parental anxiety and over-referral for stimulation programs (D’Agostino, 2010; D’Agostino, Gerdes, Manning, Phalen, & Bernabum, 2013). This idea is based on a biological-maturational perspective of development, i.e. that children born preterm would reach the level that their term peers reach during gestation only in the first years of life, following the maturation of the Central Nervous System. For these reasons authors suggest that corrected age is necessary if the child is at least under 2 years old (D’Agostino, 2010; D’Agostino et al., 2013). On the other hand, studies using CA point out that this procedure can overestimate the developmental progress in preterm infants. For example Devescovi and Capobianco measured longitudinally verbal and nonverbal skills of preterm infants with adequate weight for a gestational age between 10 and 17 months, comparing their performances to those of a group of peers born at term. The study demonstrated that the use of CA is not able to identify preterm infants’ difficulties and overestimates their abilities (Devescovi & Capobianco, 2013). In order to avoid unnecessary worries and to counterbalance the disadvantages of under- and overestimation, some authors have suggested using both ages for developmental assessment (Devescovi & Capobianco, 2013; Wilson-Ching, Pascoe, Doyle, & Anderson, 2014). Starting from the above consideration, in the present study, in order to evaluate the performances of healthy preterm children, in addition to comparing the results of premature infants to those of term-born infants, we considered both CA and UCA. This is very important because using both ages for the assessment of this population could help better identify developmental difficulties and delays in specific developmental domains without overestimating these difficulties and delays. We also better investigate how biological characteristics at birth influence the performance of premature children at 24 and 36 months. This is a relevant point because, first of all, it could better underline influences on the performance of healthy premature babies as far as the biological disadvantages at birth are concerned. Furthermore, this part of our study could be useful for clinicians because it could point out at what age one should stop using the CA. Because an early identification of neurodevelopmental delay implies an early intervention with beneficial effects on development, the first aim of this study was to assess cognitive and linguistic performance using the Bayley Scales of Infant and Toddler Development (BSID-III) in a population of healthy preterm infants, comparing the results to those of term-born infants, at 24 and 36 months, using both CA and UCA. In order to do this, we administrated BSID-III items, both at 24 and 36 months, corresponding to CA, according to the American Academy of Pediatrics guidelines (AAP, 2002) evaluating the performance of the infants using the norms for both CA and UCA. In accordance with the subset of the literature that considers preterm birth a risk factor for cognitive and linguistic development (Aarnoudse-Moens et al., 2009; Nepomnyaschy et al., 2012; Sansavini et al., 2011; Voigt, Pietz, Pauen, Kliegel, & Reuner, 2012; Woythaler, McCormick, & Smith, 2011)we expected that preterm infants would present significantly lower scores than term infants, especially using UCA. We were also interested in evaluating the possible changes between 24 and 36 months. We presumed that the gap between preterm children’s performance, considering both CA and UCA, and term children’s performance would decrease, in agreement with studies that point out that preterm children can recover from their initial disadvantage (Gurka et al., 2010). Finally, the most original part of our study was to better analyze whether the correction for prematurity should be applied and decide when to stop using corrected age. This issue is very important because the use of both ages may help to better identify where preterm infants have difficulties and to model efficient interventions for each child during the first years of life. Supposing that this correction is useful during the first two years of life (AAP, 2002; D’Agostino , 2010; D’Agostino et al., 2013) and not later, we analyzed the possible influence of GA, BW, and days of hospitalization on corrected and uncorrected

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Table 1 Characteristics of the sample.

Group

%

Preterm

Full-Term

54,7%

45,3%

Differences

62,7% 37,3%

53,2% 46,8%

␹2 = 1,245; p = 0.264

32,15 (1,97) 1631,55 (453,92) 29,70 (18,46)

39,77 (1,01) 3298,95 (457,27)

t = −21,716 p = 0.000

Gender Male Female Infant medical characteristics GA (weeks) Birth Weight (g) Hospitalization (day)

M (SD) M (SD) M (SD)

t = −17,063 p = 0.000

Note. GA = gestational age.

scores, hypothesizing that these characteristics were correlated to preterm children’s performance only at 24 months, which would confirm that the correction of prematurity is useful for the first 24 months. 2. Methods The preterm infants included in this study were part of a large cohort admitted to the Neonatal Unit of the San Raffaele Hospital of Milan between 2009 and 2012 and consecutively enrolled in a follow-up research program. The inclusion criteria were as follows: GA lower than 37 weeks and absence of congenital anomalies, major sensory impairment, severe brain injury and other neurological complications. Bilingual children were excluded. A sample of healthy term-born infants was assessed with the same follow-up protocol and used as control group. This latter group includes infants with a GA between 37 and 42 weeks with no neurological damage, birth defects, genetic syndromes, sensory impairments (visual and auditory), and behavioural disorders. Ethical approval was gained through the hospital’s research ethics committee, which required informed consent from the parents of each participant. Therefore, informed consent for the protection of privacy (Law No. 196 of 2003) was a prerequisite to participate in the study. 2.1. Participants During the study period, 62 healthy, term-born infants and 75 preterm infants fulfilled the inclusion criteria. The principal clinical characteristics of the population are reported in Table 1. Thirty-nine of the 75 preterm infants were twins. In the preterm sample the Apgar scores reported at 5 min after birth is between 7 and 10 (M = 9.5, SD= 0.85). As suggested by the American Academy of Pediatrics Committee On Fetus and Newborn (2015) the Apgar score reported at 5 min after birth provides an accepted and convenient method for reporting the status of the newborn infant immediately after birth (Watterberg et al., 2015). According to the Neonatal Encephalopathy and Neurologic Outcome report (2014) a 5-min Apgar score of 7–10 is reassuring, reflecting preterm baby’s good overall health in our sample. 2.2. Measures The BSID-III (Bayley, 2006) was used to assess the infants’ development. This instrument is widely used in preterm children’s follow-up and researches because it allowed clinicians and researchers to adjust for the child’s prematurity through 24 months of chronological age. The correction is a two-step process. First it is necessary to calculate the numbers of months and days born prematurely by subtracting the child’s date of birth from the expected date of birth. Secondly, it is necessary to subtract the adjustment for prematurity from the child’s age to obtain the corrected age. Although the BSID-III comprises five distinct scales (Cognitive, Language, Motor, Social-Emotional, and Adaptive Behavior Scales), only the Cognitive and Language Scales were administered in the present study. The Cognitive Scale (COG) includes items that assess sensorimotor development, exploration and manipulation, object relatedness, concept formation, memory, and other aspects of cognitive processing. The Language Scale (LANG) is composed of receptive communication items (Receptive Communication Subtest) and expressive communication items (Expressive Communication Subtest). The Receptive Communication Subtest (LANG RC) includes items that assess preverbal behaviors, vocabulary development, vocabulary related to morphological development, understanding of morphological markers, social referencing, and verbal comprehension. The Expressive Communication Subtest (LANG EC) includes items that assess preverbal communication, vocabulary development, and morpho-syntactic development (Greene, Patra , Nelson, & Silvestri, 2012, Greene, Patra, Silvestri, & Nelson, 2013). Infants were assessed twice: first when they reached the CA of 24 months and then at 36 months (CA). Two scores for each infant were obtained, with and without correction for preterm birth. In particular, we considered scaled scores. Scaled

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Table 2 BSID-III cognitive and language’s scores comparison between preterm CA and full term sample at 24 and 36 months. Full-Term

Preterm CA

t

p

M

SD

M

SD

24 months COG RC EC

14,55 12,32 10,84

3,486 3,116 3,125

10,46 10,42 8,94

2,312 2,568 2,115

−7, 819 −3, 694 −4, 145

0.000 0.000 0.000

36 months COG RC EC

14,92 13,54 12,96

3,285 1,749 3,026

11,35 11,25 11,09

1,828 1,391 1,442

−5, 126 −5, 758 −2980

0.000 0.000 0.000

Note. CA = corrected age; BSID-III = Bayley Scales of Infant Development third edition; COG = cognitive scale scores; RC = receptive communication scale scores; EC = expressive communication scores. Table 3 BSID-III cognitive and language’s scores comparison between preterm UCA and full term sample at 24 and 36 months. Full-Term

Preterm UCA

t

p

M

SD

M

SD

24 months COG RC EC

14,55 12,32 10,84

3,486 3,116 3,125

9,27 9,62 8,33

1,904 2,310 2,115

−10, 509 −5, 446 −5,216

0.000 0.000 0.000

36 months COG RC EC

14,92 13,54 12,96

3,285 1,749 3,026

10,95 10,93 10,37

1,779 1,399 1,458

−5, 786 −7, 225 −4,141

0.000 0.000 0.000

Note. CA = uncorrected age; BSID-III = Bayley Scales of Infant Development third edition; COG = cognitive scale scores; RC = receptive communication scale scores; EC = expressive communication scores.

scores represent children’s performance on a subtest relative to their same-age peers. They are scaled on a metric with a range of 1–19, a mean of 10, and a standard deviation of 3 (Bayley, 2006). Both populations were assessed at 24 and 36 months. All of the infants showed an examination within the normal range. 2.3. Analysis Data were analyzed with SPSS Statistics Release 20.0. Inter-group comparisons between term and preterm infants (both corrected for prematurity and uncorrected) were done by a t-test for independent sample. The intra-group comparisons between the two groups in the preterm sample (CA and UCA) for the Cognitive and Language scores were done by a t-test for paired sample. In order to evaluate the changes between 24 and 36 months, 3 new variables were created, subtracting the score obtained at 24 months from the score obtained at 36 months, for the three different groups: preterm at CA, preterm at UCA, and term. This procedure was done for each scale of the BSID-III. Comparisons were done using a univariate ANOVA, and post-hoc comparisons were done by Bonferroni’s test. Finally, considering only the preterm sample, in order to better understand the gap between CA and UCA, two other new variables were created by subtracting UCA scores from CA scores (CA-UCA) at both 24 and 36 months. These two variables were correlated with GA, BW, and days spent in hospital with a Pearson’s correlation test. The level of significance was set at p < 0.05. 3. Results In this study, we evaluated the performance of healthy preterm infants at 24 and 36 months (CA), using the BSID-III COG and LANG Scales, comparing CA and UCA results to those of term-born infants and comparing the results of CA to those of UCA. Considering the CA at both 24 and 36 months, preterm infants had significantly lower scores than those of term infants in COG and LANG (Table 2). Using UCA, preterm infants had significantly lower scores then those of term infants in both COG and LANG at 24 and 36 months (Table 3). At 24 months, significant differences between CA and UCA scores were found for both BSID-III scales. At 36 months, significant differences between CA and UCA scores were found for LANG, but not for COG (Table 4).

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Table 4 BSID-III cognitive and language’s scores comparison between preterm CA and preterm CA at 24 and 36 months. Differences between CA and UCA M

SD

t

p

24 months COG RC EC

1.222 0.839 0.516

0.941 0.578 0.805

10.31 11.423 5.051

0.000 0.000 0.000

36 moths COG RC EC

0.25 0.396 0.723

1.509 1.026 1.077

1.148 2.673 4.603

0.257 0.01 0.000

Note. UCA = uncorrected age; BSID-III = Bayley Scales of Infant Development third edition; COG = cognitive scale scores; RC = receptive communication scale scores; EC = expressive communication scores.

Fig. 1. Cognitive development between 24 and 36 months. Note. CA = corrected age; UCA = uncorrected age; BSID-III = Bayley Scales of Infant Development third edition; COG = cognitive scale scores.

Fig. 2. Receptive Communication development between 24 and 36 months. Note. CA = corrected age; UCA = uncorrected age; BSID-III = Bayley Scales of Infant Development third edition; RC = receptive communication scale scores. Table 5 Bonferroni post hoc comparisons between 24 and 36 months performance in BSID-III Cognitive scale of preterm CA, preterm UCA and full term. Differences between 24 and 36 months in COG

full-term

preterm CA preterm UCA

Mean Difference

p

−10,033 −1,8567*

0.311 0.007

We were also interested in analyzing whether there were possible significant improvements in the cognitive and linguistic performance of preterm and term children between 24 and 36 months (Figs. 1–3). In COG, the scores obtained at 24 and 36 months were statistically different (F = 4.894, P = 0.009, ␩2 = 0.075). In particular, the gap between cognitive scores significantly increased between UCA and the control group (Table 5).

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Fig. 3. Expressive Communication development between 24 and 36 months. Note. CA = corrected age; UCA = uncorrected age; BSID-III = Bayley Scales of Infant Development third edition; EC = expressive communication scores.

Finally, considering only the preterm sample, we investigated how biological characteristics at birth influence the performance of premature infants at 24 and 36 months. At 24 months, the differences between CA and UCA scores (CA – UCA) in COG and expressive communication (LANG EC) scales were significantly correlated to GA (CA – UCA in COG scale: r = −0.435, p = 0.000; CA – UCA in LANG EC scale: r = −0.326, p = 0.010) and days in the hospital (CA – UCA in COG scale: r = 0.379, p = 0.002; CA – UCA in LANG EC scale: r = 0.419, p = 0.001), and LANG EC scores were significantly correlated to BW (CA – UCA in LANG EC scale: r = −0.339, p = 0.007). At 36 months, no significant correlations were found. 4. Discussion In the present study we assessed longitudinally cognitive and linguistic performance using the BSID-III in a population of healthy preterm infants, at 24 and 36 months (CA), comparing the results of CA and UCA to those of term-born infants. Furthermore, the possible influence of GA, BW, and days of hospitalization on CA and UCA were also analyzed. Finally, we also evaluated possible changes in the performance of preterm children between 24 and 36 months. In our cohorts of preterm infants, the BSID-III showed significantly different scores from those obtained in the control group at both 24 and 36 months. These results added evidence that preterm birth is followed by poorer cognitive and language outcomes (Sansavini et al., 2011; Voigt et al., 2012; Woythaler et al., 2011). The test was performed at 24 and 36 months CA The use of this correction in preterm infants is controversial when assessing neuropsychological functions. (Aylward, 2009; Niccols & Latchman, 2002; Romeo et al., 2010; Wilson-Ching et al., 2014). No differences were found in cognitive performance between CA and UCA so if we consider only cognitive performance, these findings agree with those studies that suggest using CA until the child is 2 years old (D’Agostino, 2010; D’Agostino et al., 2013). On the contrary, without the correction, considering their linguistic performance, preterm infants obtained significantly lower scores than the control group, at both 24 and 36 months. If we also consider linguistic outcomes, our findings raise concerns about the need for age correction, considering that at later ages, as literature suggest, when correction is no longer applied, healthy preterm infants have a higher rate of developmental delay and worse school performance than term infants (Chyi et al., 2008; Morse, Zheng, Tang, & Roth, 2009; Wilson-Ching et al., 2014). We were also interested in evaluating the possible changes between 24 and 36 months. Our findings suggest that the gap between the performance of premature children obtained using CA and the performance of term children decreased. In particular, we found that with regard to cognitive development preterm children’s performances significantly improved during this brief period. This means that, in this area, preterm children seem to recover from their initial disadvantage (Gurka et al., 2010). However, as far as language development is concerned, we did not find significant improvements between preterm and term infants’ performance. In our study, none of the healthy preterm children had delays in linguistic development, however, data seem to confirm that preterm infants are at risk for language difficulties, even if their language skills seem to improve over time (Caravale et al., 2012; Guarini et al., 2009). Another interesting result of our study concerns the influence of biological characteristics at birth such as GA, BW, and the number of days spent in hospital on both CA and UCA. We found that these characteristics were correlated to preterm performance only at 24 months, which may confirm that the correction of prematurity is useful until 24 months, but not later. At 24 months, we found that lower GA, lower BW, and more days spent in hospital correlated with a larger gap between corrected and chronological scores. We did not find any correlation at 36 months. The use of both CA and UCA in our study allowed us to confirm that considering both CA and UCA during preterm infants follow-up is important as it helps clinicians to better identify which areas are more problematic during their development, without overestimating impairments in their performance. This could also help to model more efficient interventions for each child during his or her first years of life. Furthermore, specific neuropsychological domains such as cognitive and linguistic processes were considered. This allowed us to highlight frequent difficulties in healthy preterm infants that are normally

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considered “healthy”. Finally, even the longitudinal design was useful to better analyze significant differences between 24and 36-month performances and in order to understand when to stop using the correction for prematurity. This study had some limitations. First, we involved a limited sample size, so we cannot say how far our findings can be generalized to the broader population of children born preterm. Furthermore, another important limitation is that there is not an Italian validation of the normative values of the BSID-III (Bayley, 2006). We obtained the normative value from the U.S. validation. This could be a limit, especially in language assessment, since the acquisition and learning of English and Italian languages is not quite comparable and some linguistic structures could be acquired or learned in different ways and at different times (Caselli et al., 1995). 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