Do preschoolers born premature perform properly on lexical and verbal short-term memory abilities?

Marianne Querido Verreschi Ana Manhani Cáceres-Assenço Vera Lúcia Jornada Krebs Werther Brunow de Carvalho Debora Maria Befi-Lopes About the authors

RESUMO

Objetivo

Investigar o desempenho lexical e a habilidade de memória de curto prazo verbal em crianças prematuras em idade pré-escolar, e comparar os resultados com seus pares nascidos a termo.

Método

Participaram do estudo 40 pré-escolares com idade entre 4 e 5 anos e 11 meses divididos em dois grupos, sendo 20 nascidos prematuros e 20 nascidos a termo. Os grupos não diferiram quanto à idade, renda familiar e escolaridade materna. Foram utilizados testes de vocabulário expressivo e memória de curto prazo verbal. A análise estatística inferencial foi realizada por meio dos testes de Mann-Whitney e exato de Fisher.

Resultados

O desempenho dos grupos não diferiu na tarefa de vocabulário, mas o grupo de prematuros apresentou desempenho inferior ao de seus pares na tarefa de repetição de não palavras.

Conclusão

Nesta amostra, o desempenho dos pré-escolares que nasceram prematuros foi estatisticamente inferior ao daqueles nascidos a termo apenas na tarefa de repetição de não palavras. Assim, o nascimento prematuro esteve associado a desempenho no vocabulário expressivo compatível com o esperado para a idade, porém com prejuízos na memória de curto prazo verbal.

Descritores:
Recém-Nascido Prematuro; Linguagem Infantil; Linguagem; Vocabulário; Memória

ABSTRACT

Purpose

To investigate lexical performance and verbal short-term memory ability in premature infants at preschool age and compare the results with their full-term peers.

Methods

Forty preschool children aged between 4 and 5 years and 11 months participated on the study and were equally divided into two groups considering their gestational age: preterm and full-term. Groups did not differ on age, family income and maternal education. Participants were paired according to their chronological age and their socioeconomic status. Their performance was assessed using expressive vocabulary and verbal short-term memory tests. Inferential statistical analysis was performed using the Mann-Whitney and the Fisher exact test.

Results

Group performance did not differ on vocabulary, but premature children showed an inferior performance on nonword repetition tasks.

Conclusion

These data indicates that preschoolers born premature performed statistically lower than their peers born full-term on nonword repetition task. Thus, premature birth was associated to vocabulary development on typically developing range, but also to verbal short-term memory impairments.

Keywords:
Infant, Premature; Child Language; Language; Vocabulary; Memory

INTRODUCTION

A birth is considered premature when occurs before the pregnancy reaches 37 weeks(11 SBP: Sociedade Brasileira de Pediatria. Prevenção da prematuridade: uma intervenção da gestão e da assistência. Rio de Janeiro: Departamento Científico de Neonatologia, Sociedade Brasileira de Pediatria; 2017. p. 1-6. (Documento científico; 2).) from the date of the woman's last menstruation, and is the leading cause of neonatal death worldwide(22 WHO: World Health Organization [Internet]. Preterm birth. Switzerland: WHO; 2017 [citado em 2018 Jan 18]. Disponível em: http://www.who.int/mediacentre/factsheets/fs363/en/
http://www.who.int/mediacentre/factsheet...
). According to the World Health Organization (WHO), about 15 million babies are born prematurely each year.

Babies can be classified as premature according to their gestational age: extreme preterm (gestational age less than 28 weeks), very preterm (from 28 weeks and 0 days to 31 weeks and 6 days), moderate preterm (32 weeks and 0 days to 33 weeks and 6 days), and late preterm (34 weeks and 0 days to 36 weeks and 6 days)(11 SBP: Sociedade Brasileira de Pediatria. Prevenção da prematuridade: uma intervenção da gestão e da assistência. Rio de Janeiro: Departamento Científico de Neonatologia, Sociedade Brasileira de Pediatria; 2017. p. 1-6. (Documento científico; 2).).

Birth weight is another variable often related to prematurity. Newborns weighing less than 2500 grams are considered low weight, those born less than 1500 grams are considered very low weight, and those born less than 1000 grams are considered extremely low weight(33 Tavares EC, Rego MAS. Prematuridade e crescimento fetal restrito. In: Lopes FA, Campo D Jr. Tratado de pediatria: sociedade brasileira de pediatria. 2. ed. Barueri: Manole; 2010. p. 1445-54.).

It is also possible to classify newborns according to their weight/gestational age ratio. For each gestational age, there is a normal weight variation between the 10th and 90th percentiles for a given population. The categories are BGA (big for gestational age), above the 90th percentile; AGA (appropriate for gestational age), between the 10th and 90th percentiles; SGA (small for gestational age), below the 10th percentile(33 Tavares EC, Rego MAS. Prematuridade e crescimento fetal restrito. In: Lopes FA, Campo D Jr. Tratado de pediatria: sociedade brasileira de pediatria. 2. ed. Barueri: Manole; 2010. p. 1445-54.).

Prematurity and low birth weight are biological risk factors for children development(44 Nobre FDA, Carvalho AEV, Martinez FEM, Linhares MBM. Estudo longitudinal do desenvolvimento de crianças nascidas pré-termo no primeiro ano pós-natal. Psicol Reflex Crit. 2009;22(3):362-69. http://dx.doi.org/10.1590/S0102-79722009000300006.
http://dx.doi.org/10.1590/S0102-79722009...
,55 Silveira RC. Seguimento ambulatorial do prematuro de risco. 1. ed. Porto Alegre: Sociedade Brasileira de Pediatria. Departamento Científico de Neonatologia; 2012.). In the first years of life, preterm infants may have impaired motor, cognitive, and language development compared to term infants(44 Nobre FDA, Carvalho AEV, Martinez FEM, Linhares MBM. Estudo longitudinal do desenvolvimento de crianças nascidas pré-termo no primeiro ano pós-natal. Psicol Reflex Crit. 2009;22(3):362-69. http://dx.doi.org/10.1590/S0102-79722009000300006.
http://dx.doi.org/10.1590/S0102-79722009...

5 Silveira RC. Seguimento ambulatorial do prematuro de risco. 1. ed. Porto Alegre: Sociedade Brasileira de Pediatria. Departamento Científico de Neonatologia; 2012.

6 Ishii C, Miranda CS, Isotani SM, Perissinoto J. Characterization of linguistic behaviors of premature four-year old children. Rev CEFAC. 2006;8(2):147-54.

7 Vieira MEB, Linhares MBM. Developmental outcomes and qualify of life in children born preterm at preschol and school-age. J Pediatr (Rio J). 2011;87(4):281-91. http://dx.doi.org/10.2223/JPED.2096. PMid:21743941.
http://dx.doi.org/10.2223/JPED.2096...

8 Fernandes LV, Goulart AL, Santos AMN, Barros MC, Guerra CC, Kopelman BI. Neurodevelopmental assessment of very low birth wight preterm infants at corrected age of 18-24 months by Bayley III scales. J Pediatr (Rio J). 2012;88(6):471-8. PMid:23172131.

9 Sansavini A, Pentimonti J, Justice L, Guarini A, Savini S, Alessandroni R, et al. Language, motor and cognitive development of extremely preterm children: modeling individual growth trajectories over the first three years of life. J Commun Disord. 2014;49:55-68. http://dx.doi.org/10.1016/j.jcomdis.2014.02.005. PMid:24630591.
http://dx.doi.org/10.1016/j.jcomdis.2014...

10 Maggiolo ML, Varela VM, Arancibia CS, Ruiz FM. Dificultades de lenguaje en niños preescolares con antecedente de prematuridad extrema. Rev Chil Pediatr. 2014;85(3):319-27. http://dx.doi.org/10.4067/S0370-41062014000300008. [Internet]
http://dx.doi.org/10.4067/S0370-41062014...

11 Guarini A, Marini A, Savini S, Alessandroni R, Faldella G, Sansavini A. Linguistic features in children born very preterm at preschool age. Dev Med Child Neurol. 2016;58(9):949-56. http://dx.doi.org/10.1111/dmcn.13118. PMid:27061384.
http://dx.doi.org/10.1111/dmcn.13118...
-1212 Ribeiro CD, Pachelli MR, Amaral NC, Lamônica DA. Development skills of children born premature with low and very low birth weight. CoDAS. 2017;29(1):e20160058. PMid:28146204.).

Changes have been reported in the language development, such as late-onset of first-word utterance, delay in expanding vocabulary and linguistic functionality(66 Ishii C, Miranda CS, Isotani SM, Perissinoto J. Characterization of linguistic behaviors of premature four-year old children. Rev CEFAC. 2006;8(2):147-54.,1313 Costa Ribeiro C, Abramides DV, Fuertes MG, Lopes dos Santos PN, Lamônica DA. Receptive language and intellectual abilities in preterm children. Early Hum Dev. 2016;99:57-60. http://dx.doi.org/10.1016/j.earlhumdev.2016.03.011. PMid:27415774.
http://dx.doi.org/10.1016/j.earlhumdev.2...
), and difficulties with grammatical, phonological, pragmatic and linguistic comprehension skills(44 Nobre FDA, Carvalho AEV, Martinez FEM, Linhares MBM. Estudo longitudinal do desenvolvimento de crianças nascidas pré-termo no primeiro ano pós-natal. Psicol Reflex Crit. 2009;22(3):362-69. http://dx.doi.org/10.1590/S0102-79722009000300006.
http://dx.doi.org/10.1590/S0102-79722009...
,1010 Maggiolo ML, Varela VM, Arancibia CS, Ruiz FM. Dificultades de lenguaje en niños preescolares con antecedente de prematuridad extrema. Rev Chil Pediatr. 2014;85(3):319-27. http://dx.doi.org/10.4067/S0370-41062014000300008. [Internet]
http://dx.doi.org/10.4067/S0370-41062014...
,1111 Guarini A, Marini A, Savini S, Alessandroni R, Faldella G, Sansavini A. Linguistic features in children born very preterm at preschool age. Dev Med Child Neurol. 2016;58(9):949-56. http://dx.doi.org/10.1111/dmcn.13118. PMid:27061384.
http://dx.doi.org/10.1111/dmcn.13118...
). In some cases, these issues may appear in the preschool and school stages and last for a lifetime(55 Silveira RC. Seguimento ambulatorial do prematuro de risco. 1. ed. Porto Alegre: Sociedade Brasileira de Pediatria. Departamento Científico de Neonatologia; 2012.,66 Ishii C, Miranda CS, Isotani SM, Perissinoto J. Characterization of linguistic behaviors of premature four-year old children. Rev CEFAC. 2006;8(2):147-54.,1010 Maggiolo ML, Varela VM, Arancibia CS, Ruiz FM. Dificultades de lenguaje en niños preescolares con antecedente de prematuridad extrema. Rev Chil Pediatr. 2014;85(3):319-27. http://dx.doi.org/10.4067/S0370-41062014000300008. [Internet]
http://dx.doi.org/10.4067/S0370-41062014...
,1414 Boyer J, Flamant C, Boussicault G, Berlie I, Gascoin G, Branger B, et al. Characterizing early detection of language difficulties in children born preterm. Early Hum Dev. 2014;90(6):281-6. http://dx.doi.org/10.1016/j.earlhumdev.2014.03.005. PMid:24726534.
http://dx.doi.org/10.1016/j.earlhumdev.2...
,1515 Zerbeto AB, Cortelo FM, Filho EBC. Association between gestational age and birth weight on the language development of Brazilian children: A systematic review. J Pediatr (Rio J). 2015;91(4):326-32. http://dx.doi.org/10.1016/j.jped.2014.11.003. PMid:25913048.
http://dx.doi.org/10.1016/j.jped.2014.11...
).

In addition to the impact on language development, other cognitive skills such as memory may also have their development affected. Recent studies have shown that premature children performed worse than their full-term peers on verbal short-term memory tasks, such as non-word repetition and digit span(1111 Guarini A, Marini A, Savini S, Alessandroni R, Faldella G, Sansavini A. Linguistic features in children born very preterm at preschool age. Dev Med Child Neurol. 2016;58(9):949-56. http://dx.doi.org/10.1111/dmcn.13118. PMid:27061384.
http://dx.doi.org/10.1111/dmcn.13118...
) and verbal working memory(1616 Riva V, Cantiani C, Dionne G, Marini A, Mascheretti S, Molteni M, et al. Working memory mediates the effects of gestational age at birth on expressive language development in children. Neuropsychology. 2017;31(5):475-85. http://dx.doi.org/10.1037/neu0000376. PMid:28383969.
http://dx.doi.org/10.1037/neu0000376...
).

Verbal short-term memory is directly related to language acquisition and comprehension. It supports the formation and stabilization of phonological representations of new words in long-term memory, being related to morphosyntactic and functional learning, and the understanding of short narrative sentences(1717 Baddeley A. Working memory. Curr Biol. 2010;20(4):R136-40. http://dx.doi.org/10.1016/j.cub.2009.12.014. PMid:20178752.
http://dx.doi.org/10.1016/j.cub.2009.12....

18 Vugs B, Knoors H, Cuperus J, Hendriks M, Verhoeven L. Interactions between working memory and language in young children with Specific Language Impairment (SLI). Child Neuropsychol. 2015;22(8):1-24. PMid:26144244.

19 Montgomery JW, Magimairaj BM, Finney MC. Working memory and specific language impairment: an update on the relation and perspectives on assessment and treatment. Am J Speech Lang Pathol. 2010;19(1):78-94. http://dx.doi.org/10.1044/1058-0360(2009/09-0028). PMid:19948760.
http://dx.doi.org/10.1044/1058-0360(2009...
-2020 Engel de Abreu PMJ, Gathercole SE, Martin R. Disentangling the relationship between working memory and language: the roles of short-term storage and cognitive control. Learn Individ Differ. 2011;21(5):569-74. http://dx.doi.org/10.1016/j.lindif.2011.06.002.
http://dx.doi.org/10.1016/j.lindif.2011....
).

Studies on language development and verbal short-term memory in preterm infants are scarce(1111 Guarini A, Marini A, Savini S, Alessandroni R, Faldella G, Sansavini A. Linguistic features in children born very preterm at preschool age. Dev Med Child Neurol. 2016;58(9):949-56. http://dx.doi.org/10.1111/dmcn.13118. PMid:27061384.
http://dx.doi.org/10.1111/dmcn.13118...
) and predominantly international. Investigating these skills in the Brazilian context is relevant to deepen the understanding of prematurity in the development of communication in early childhood and, especially, to investigate whether this population is at higher risk for developing neurodevelopmental disorders that will impact their learning. Thus, this study aimed to verify lexical performance and verbal short-term memory ability in preschool children (4 to 5 years and 11 months old) born prematurely and to compare the results with their full-term peers.

METHODS

The Research Ethics Committee of the Institution approved this study under number 53465416.0.0000.0068. All individuals agreed to participate in the study through graphic registration and had an informed consent signed by their guardians.

Participants

The study included a research group (RG) and a control group (CG). Individuals in both groups were aged between 4 years and 5 years and 11 months old (average RG 61.0 ±7.41 months old; average CG 61.4 ±4.86; p=0.841). As it was a convenience sample, the groups were matched by age with up to six months variation. This variation occurred because, despite the individuals matched by date of birth, they underwent data collection at different times. The RG was composed of eight 4-year-old and twelve 5-year-old individuals with an age range between 48 and 71 months, while the CG was composed of seven 4-year-old and thirteen 5-year-old individuals with age range between 53 to 68 months. Although the RG had greater age variation in months than the CG, the groups did not differ by age.

Family socioeconomic status was characterized by monthly incomes (median RG R$ 3000.00; interquartile range (IQ) 2125.00 - 5000.00; median CG R$ 2000.00 IQ1500.00 - 4000.00; p = 0.147) and maternal education level (85% of mothers completed at least high school in both groups). The groups also did not differ regarding monthly family income and maternal education.

The research group (RG) was composed according to the demand of the ICr-HCFMUSP Newborn at Risk Follow-up of the Neonatal Center. Twenty preschoolers of both genders (ten boys), premature and under pediatric outpatient follow-up during the data collection period, were evaluated. Of those, 85% attended preschool regularly, and none underwent speech therapy.

The eligibility criteria included gestational age of less than 37 complete weeks; absence of sensory deprivation, neurological changes, and developmental diagnoses that could interfere with language acquisition and development.

The participants clinical data were consulted through analysis of electronic medical records. We considered information related to gestational age, type of delivery, birth weight, gestational age/weight ratio, height, head circumference, Apgar score, and length of stay.

Regarding the classification of prematurity(11 SBP: Sociedade Brasileira de Pediatria. Prevenção da prematuridade: uma intervenção da gestão e da assistência. Rio de Janeiro: Departamento Científico de Neonatologia, Sociedade Brasileira de Pediatria; 2017. p. 1-6. (Documento científico; 2).), the sample consisted of 55% very preterm, 30% moderate preterm, 10% late preterm, and 5% extreme preterm. Regarding birth weight, 15% of the individuals were extremely underweight, and 45% of the individuals were classified as SGA. Due to the highlighted variability, these variables were not considered in the analyses of this article (Chart 1).

Chart 1
Characterization of the group of premature children

The control group (CG) was composed of 20 preschool children with typical language development, born at term, within the same age range as the research group, both genders (14 boys), regularly enrolled in a public kindergartens in the west of São Paulo. The inclusion criteria included gestational age equal or greater than 37 complete weeks, absence of complaints, referral or attendance in force for speech, psychological or neurological demands of diagnosed conditions that could interfere with language acquisition and development (Chart 2).

Chart 2
Characterization of the group of children born at term

Materials and procedures

Data collection from the research group was performed in a silent office at the ICr-HCFMUSP Clinical Research Center, and the data collection from the control group was performed in a silent classroom at the school. In both cases, the children interacted with the researcher and all procedures were performed in a single session, with an average duration of 20 minutes, recorded on a digital recorder for later transcription.

We used the Expressive Vocabulary Test - ABFW(2121 Befi-Lopes DM. Vocabulário. In: Andrade CRFD, Befi-Lopes DM, Fernandes FDM, Wertzner HF, editores. ABFW: teste de linguagem infantil nas áreas de fonologia, vocabulário, fluência e pragmática. 2. ed. Barueri: Pró-Fono; 2004. p. 33-50.) to investigate lexical development, consisting of 118 figures divided into nine semantic fields: clothing, food, animals, means of transport, furniture and utensils, professions, places, shapes and colors, toys and musical instruments. The analysis classifies the answers into usual verbal designations (UVD), non-designations (ND), and substitution processes (SP), giving the percentage of correct answers in each semantic field, with normality pattern. The test followed the instructions available in the user manual. For this study, the analysis considered the total percentage of usual verbal designation (UVD), which corresponds to the sum of the UVD of all semantic fields divided by the total number of test items and multiplied by 100.

We used the Phonological Short-Term Memory test(2222 Rodrigues A, Befi-Lopes DM. Short-term phonological memory in preschool children. CoDAS. 2013;25(5):422-8. http://dx.doi.org/10.1590/S2317-17822013000500005. PMid:24408545.
http://dx.doi.org/10.1590/S2317-17822013...
) to investigate verbal short-term memory ability, composed of 40 non-words divided equally into groups of monosyllables, disyllables, trisyllables, and polysyllables. For this study, we considered the total percentage of correct answers, which corresponds to the sum of the correct answers in the different syllable extensions of non-words divided by the total number of items and multiplied by 100.

The individuals’ performance was considered “adequate” when it reached the performance parameters indicated by age in both instruments, and considered “inadequate” when below the expectations.

The individuals of the research group were characterized regarding pregnancy and birth factors: maternal diseases (diabetes, hypertension, others), gestational age, type of delivery, birth weight, length of stay, clinical status (occurrence of neonatal jaundice, time of phototherapy, infections, intracranial hemorrhage, others). These factors were obtained from the analysis of the electronic records of the outpatient clinic mentioned above.

The control group was also characterized as to gestational and birth factors, through a questionnaire answered by their parents and/or guardians.

To characterize and pair the researched groups, we measured family socioeconomic aspects by a questionnaire based on the Brazil Economic Classification Criteria(2323 ABEP: Associação Brasileira de Empresas de Pesquisa [Internet]. Critério Brasil: Critério de Classificação Econômica Brasil 2013: base LSE 2011. São Paulo: ABEP; 2013 [citado em 2017 Abr 22]. Disponível em: www.abep.org/criterio-brasil
www.abep.org/criterio-brasil...
), answered by the participants’ guardians.

We recorded all the data through the specific protocols of each test, transcribed and also stored in digital voice file.

Statistical analysis

The data were analyzed with the software SPSS version 21. Descriptive analysis of categorical variables occurred by the gross value and its distribution frequency. Numerical variables were described by the median and interquartile range when the distribution did not respect normality, and by the mean and standard deviation when the distribution respected normality. The individuals’ performance was compared with inferential analysis by the nonparametric Mann-Whitney test; and Fisher's exact test compared the frequency distribution of the performance classification between the groups. The adopted significance level was 5%.

RESULTS

The research and control groups were characterized by their gestational data - maternal and fetal - and data at birth, as can be observed in Tables 1 and 2.

Table 1
Comparison of group performance (score) in expressive vocabulary and verbal short-term memory tasks
Table 2
Comparison of group performance classification in expressive vocabulary and verbal short-term memory tasks

When comparing the groups’ performance, the preterm infants performed similarly to their peers in the vocabulary test but presented inferior performance in the verbal short-term memory. However, even in the case of vocabulary, the values of the interquartile range of preterm infants are lower compared to the control group in the first and third quartiles (Table 1).

By analyzing only the research group, we compared the performance of individuals classified as AGA or SGA, since the latter would present a higher risk for developmental changes. However, there was no difference between individuals in the percentage of vocabulary UVD (median AGA 64, median SGA 69, p = 0.062), nor in the percentage of verbal short-term memory hits (median AGA 83, median SGA 85, p = 0.152). When comparing the vocabulary performance classification, three (27.3%) AGA and only one (11.1%) SGA participants were inadequate, which was not statistically significant (p = 0.375). In verbal short-term memory, seven (63.6%) AGA and six (66.7%) SGA participants were inadequate, which also does not configure a statistical difference (p = 0.630).

When comparing the groups’ performance classification in each evaluated domain, we observed no association between the group and the vocabulary classification; i.e., the distribution of individuals in the classifications is similar in both groups. In verbal short-term memory, preterm infants had their performance rated as less adequate than their peers (Table 2).

DISCUSSION

This research aimed to verify the performance of children between 4 and 5 years and 11 months old with a history of prematurity in vocabulary tasks and verbal short-term memory and to compare it with their term peers.

We observed no statistical difference between the groups in the expressive vocabulary, either by the total percentage of UVD or by the performance rating. This result differs from previous studies that showed difficulties with expressive and receptive vocabulary in preterm children in different age groups(99 Sansavini A, Pentimonti J, Justice L, Guarini A, Savini S, Alessandroni R, et al. Language, motor and cognitive development of extremely preterm children: modeling individual growth trajectories over the first three years of life. J Commun Disord. 2014;49:55-68. http://dx.doi.org/10.1016/j.jcomdis.2014.02.005. PMid:24630591.
http://dx.doi.org/10.1016/j.jcomdis.2014...
,1010 Maggiolo ML, Varela VM, Arancibia CS, Ruiz FM. Dificultades de lenguaje en niños preescolares con antecedente de prematuridad extrema. Rev Chil Pediatr. 2014;85(3):319-27. http://dx.doi.org/10.4067/S0370-41062014000300008. [Internet]
http://dx.doi.org/10.4067/S0370-41062014...
,1313 Costa Ribeiro C, Abramides DV, Fuertes MG, Lopes dos Santos PN, Lamônica DA. Receptive language and intellectual abilities in preterm children. Early Hum Dev. 2016;99:57-60. http://dx.doi.org/10.1016/j.earlhumdev.2016.03.011. PMid:27415774.
http://dx.doi.org/10.1016/j.earlhumdev.2...
). In two of these studies, children aged 12 to 36 months old with a history of extreme and moderate prematurity(99 Sansavini A, Pentimonti J, Justice L, Guarini A, Savini S, Alessandroni R, et al. Language, motor and cognitive development of extremely preterm children: modeling individual growth trajectories over the first three years of life. J Commun Disord. 2014;49:55-68. http://dx.doi.org/10.1016/j.jcomdis.2014.02.005. PMid:24630591.
http://dx.doi.org/10.1016/j.jcomdis.2014...
,1313 Costa Ribeiro C, Abramides DV, Fuertes MG, Lopes dos Santos PN, Lamônica DA. Receptive language and intellectual abilities in preterm children. Early Hum Dev. 2016;99:57-60. http://dx.doi.org/10.1016/j.earlhumdev.2016.03.011. PMid:27415774.
http://dx.doi.org/10.1016/j.earlhumdev.2...
) were analyzed, while the other study evaluated children aged 4 to 5 years old and with a history of extreme prematurity(1010 Maggiolo ML, Varela VM, Arancibia CS, Ruiz FM. Dificultades de lenguaje en niños preescolares con antecedente de prematuridad extrema. Rev Chil Pediatr. 2014;85(3):319-27. http://dx.doi.org/10.4067/S0370-41062014000300008. [Internet]
http://dx.doi.org/10.4067/S0370-41062014...
). Therefore, both the difference in gestational age and the age of the children at the time of research may justify the divergence observed between the results presented since. Our study shows a predominance of gestational age between 28 weeks and 0 days to 33 weeks and six days.

However, these findings corroborated with two international studies(2424 Pérez-Pereira M, Fernández P, Gómez-Taibo ML, Resches M. Language development of low risk preterm infants up to the age of 30 months. Early Hum Dev. 2014;90(10):649-56. http://dx.doi.org/10.1016/j.earlhumdev.2014.08.004. PMid:25189697.
http://dx.doi.org/10.1016/j.earlhumdev.2...
,2525 Coletti MF, Caravale B, Gasparini C, Franco F, Campi F, Dotta A. One-year neurodevelopmental outcome of very and late preterm infants: risk factors and correlation with maternal stress. Infant Behav Dev. 2015;39:11-20. http://dx.doi.org/10.1016/j.infbeh.2015.01.003. PMid:25779697.
http://dx.doi.org/10.1016/j.infbeh.2015....
). In the first study, the longitudinal comparison of language development at 10, 22, and 30 months of children with and without a history of premature birth found no statistical difference between the groups in comprehension and production of words, phrases, communicative, and cognitive skills(2424 Pérez-Pereira M, Fernández P, Gómez-Taibo ML, Resches M. Language development of low risk preterm infants up to the age of 30 months. Early Hum Dev. 2014;90(10):649-56. http://dx.doi.org/10.1016/j.earlhumdev.2014.08.004. PMid:25189697.
http://dx.doi.org/10.1016/j.earlhumdev.2...
). Another study showed no statistical difference was observed between preterm and term children in cognitive, language and motor tasks at 12 months of corrected age. However, their research group consisted of healthy individuals with no clinical risk, so that, even with different gestational ages (very preterm and late preterm), all of them achieved scores adequate to the experimental test parameters(2525 Coletti MF, Caravale B, Gasparini C, Franco F, Campi F, Dotta A. One-year neurodevelopmental outcome of very and late preterm infants: risk factors and correlation with maternal stress. Infant Behav Dev. 2015;39:11-20. http://dx.doi.org/10.1016/j.infbeh.2015.01.003. PMid:25779697.
http://dx.doi.org/10.1016/j.infbeh.2015....
).

The individuals of this research did not differ as much by chronological age as by family socioeconomic level, nor did they present high-risk clinical conditions, meeting the eligibility criteria already mentioned. However, the literature used as reference uses similar eligibility criteria, i.e., the aspects in which there is a divergence from the literature cannot be justified by the possibility of comparisons with premature children with high clinical risk for developmental changes(44 Nobre FDA, Carvalho AEV, Martinez FEM, Linhares MBM. Estudo longitudinal do desenvolvimento de crianças nascidas pré-termo no primeiro ano pós-natal. Psicol Reflex Crit. 2009;22(3):362-69. http://dx.doi.org/10.1590/S0102-79722009000300006.
http://dx.doi.org/10.1590/S0102-79722009...
,66 Ishii C, Miranda CS, Isotani SM, Perissinoto J. Characterization of linguistic behaviors of premature four-year old children. Rev CEFAC. 2006;8(2):147-54.

7 Vieira MEB, Linhares MBM. Developmental outcomes and qualify of life in children born preterm at preschol and school-age. J Pediatr (Rio J). 2011;87(4):281-91. http://dx.doi.org/10.2223/JPED.2096. PMid:21743941.
http://dx.doi.org/10.2223/JPED.2096...

8 Fernandes LV, Goulart AL, Santos AMN, Barros MC, Guerra CC, Kopelman BI. Neurodevelopmental assessment of very low birth wight preterm infants at corrected age of 18-24 months by Bayley III scales. J Pediatr (Rio J). 2012;88(6):471-8. PMid:23172131.

9 Sansavini A, Pentimonti J, Justice L, Guarini A, Savini S, Alessandroni R, et al. Language, motor and cognitive development of extremely preterm children: modeling individual growth trajectories over the first three years of life. J Commun Disord. 2014;49:55-68. http://dx.doi.org/10.1016/j.jcomdis.2014.02.005. PMid:24630591.
http://dx.doi.org/10.1016/j.jcomdis.2014...

10 Maggiolo ML, Varela VM, Arancibia CS, Ruiz FM. Dificultades de lenguaje en niños preescolares con antecedente de prematuridad extrema. Rev Chil Pediatr. 2014;85(3):319-27. http://dx.doi.org/10.4067/S0370-41062014000300008. [Internet]
http://dx.doi.org/10.4067/S0370-41062014...

11 Guarini A, Marini A, Savini S, Alessandroni R, Faldella G, Sansavini A. Linguistic features in children born very preterm at preschool age. Dev Med Child Neurol. 2016;58(9):949-56. http://dx.doi.org/10.1111/dmcn.13118. PMid:27061384.
http://dx.doi.org/10.1111/dmcn.13118...

12 Ribeiro CD, Pachelli MR, Amaral NC, Lamônica DA. Development skills of children born premature with low and very low birth weight. CoDAS. 2017;29(1):e20160058. PMid:28146204.

13 Costa Ribeiro C, Abramides DV, Fuertes MG, Lopes dos Santos PN, Lamônica DA. Receptive language and intellectual abilities in preterm children. Early Hum Dev. 2016;99:57-60. http://dx.doi.org/10.1016/j.earlhumdev.2016.03.011. PMid:27415774.
http://dx.doi.org/10.1016/j.earlhumdev.2...

14 Boyer J, Flamant C, Boussicault G, Berlie I, Gascoin G, Branger B, et al. Characterizing early detection of language difficulties in children born preterm. Early Hum Dev. 2014;90(6):281-6. http://dx.doi.org/10.1016/j.earlhumdev.2014.03.005. PMid:24726534.
http://dx.doi.org/10.1016/j.earlhumdev.2...

15 Zerbeto AB, Cortelo FM, Filho EBC. Association between gestational age and birth weight on the language development of Brazilian children: A systematic review. J Pediatr (Rio J). 2015;91(4):326-32. http://dx.doi.org/10.1016/j.jped.2014.11.003. PMid:25913048.
http://dx.doi.org/10.1016/j.jped.2014.11...
-1616 Riva V, Cantiani C, Dionne G, Marini A, Mascheretti S, Molteni M, et al. Working memory mediates the effects of gestational age at birth on expressive language development in children. Neuropsychology. 2017;31(5):475-85. http://dx.doi.org/10.1037/neu0000376. PMid:28383969.
http://dx.doi.org/10.1037/neu0000376...
,2424 Pérez-Pereira M, Fernández P, Gómez-Taibo ML, Resches M. Language development of low risk preterm infants up to the age of 30 months. Early Hum Dev. 2014;90(10):649-56. http://dx.doi.org/10.1016/j.earlhumdev.2014.08.004. PMid:25189697.
http://dx.doi.org/10.1016/j.earlhumdev.2...
,2626 Linsell L, Malouf R, Morris J, Kurinczuk JJ, Marlow N. Prognostic factors for poor cognitive development in children born very preterm or with very low birth weight: a systematic review. JAMA Pediatr. 2015;169(12):1162-72. http://dx.doi.org/10.1001/jamapediatrics.2015.2175. PMid:26457641.
http://dx.doi.org/10.1001/jamapediatrics...
).

Environmental factors may also interfere with the language performance of premature children. In children below five years old who were born too premature or small for gestational age, factors such as low parental education, low birth weight, and male gender may act as predictors of changes in overall cognitive development. From five years old, only the influence of parents' educational level seems to be sustained, suggesting that the influence of perinatal risk factors decreases over time and that the social and environmental factors become more important(2626 Linsell L, Malouf R, Morris J, Kurinczuk JJ, Marlow N. Prognostic factors for poor cognitive development in children born very preterm or with very low birth weight: a systematic review. JAMA Pediatr. 2015;169(12):1162-72. http://dx.doi.org/10.1001/jamapediatrics.2015.2175. PMid:26457641.
http://dx.doi.org/10.1001/jamapediatrics...
).

Although many studies have shown a risk of impaired language development in premature children, developmental recovery may occur throughout the maturation of the nervous system, in the absence of brain damage, and when the child interacts with the healthy environment around him(1313 Costa Ribeiro C, Abramides DV, Fuertes MG, Lopes dos Santos PN, Lamônica DA. Receptive language and intellectual abilities in preterm children. Early Hum Dev. 2016;99:57-60. http://dx.doi.org/10.1016/j.earlhumdev.2016.03.011. PMid:27415774.
http://dx.doi.org/10.1016/j.earlhumdev.2...
). Thus, considering that in this study most premature children attended kindergartens regularly, as provided for in Brazilian legislation for children of this age group, it is possible that this factor contributed to the development of language, specifically lexical acquisition, which could justify similar performance with term-born children who also attend kindergarten.

However, despite the absence of statistical difference, the median obtained in the group of premature infants indicated a narrower performance than children born at term. This result may be due to familiarity with the task and the items, but it does not necessarily imply that performance would be the same with less frequent lexical elements, which may impact the future academic performance of these children. Only the isolated vocabulary task is not able to evaluate the linguistic performance of these groups and allows discussion only about vocabulary.

Another relevant aspect to be considered in this group is that the sample is composed of 30% of twins and 45% of infants born small for gestational age, which increases the risk for language development disorders(2727 Taylor CA, Rice ML, Christensen D, Blair E, Zubrick SR. Prenatal and perinatal risks for late language emergence in a population-level sample of twins at age 2. BMC Pediatr. 2018;18(1):41. http://dx.doi.org/10.1186/s12887-018-1035-9. PMid:29415681.
http://dx.doi.org/10.1186/s12887-018-103...
,2828 Goto MMF, Gonçalves VMG, Netto AA, Morcillo AM, Moura-Ribeiro MVL. Neurodesenvolvimento de lactentes nascidos a termo pequenos para a idade gestacional no segundo mês de vida. Arq Neuropsiquiatr. 2005;63(1):75-82. http://dx.doi.org/10.1590/S0004-282X2005000100014. PMid:15830069.
http://dx.doi.org/10.1590/S0004-282X2005...
). A recent study(2727 Taylor CA, Rice ML, Christensen D, Blair E, Zubrick SR. Prenatal and perinatal risks for late language emergence in a population-level sample of twins at age 2. BMC Pediatr. 2018;18(1):41. http://dx.doi.org/10.1186/s12887-018-1035-9. PMid:29415681.
http://dx.doi.org/10.1186/s12887-018-103...
) presented a multivariate analysis regarding the association of perinatal and postnatal factors with delayed twin language development. The results indicated an association of perinatal factors, such as gestational diabetes and monozygotic pregnancy, but postnatal factors, such as socioeconomic status and maternal education, were not associated with delayed language development.

When comparing the classification of the groups' performance in vocabulary, the statistical significance was borderline, probably due to the sample size. Therefore, we need to be careful when generalizing these data, since. A larger sample size could be able to replicate the difference in vocabulary performance of premature and term infants observed by other authors.

Children born prematurely presented verbal short-term memory performance impairments. This finding corroborates with an Italian study that points out that premature children had difficulties with this ability and other cognitive abilities, detected from the age of three, and observed in children of five years old(1111 Guarini A, Marini A, Savini S, Alessandroni R, Faldella G, Sansavini A. Linguistic features in children born very preterm at preschool age. Dev Med Child Neurol. 2016;58(9):949-56. http://dx.doi.org/10.1111/dmcn.13118. PMid:27061384.
http://dx.doi.org/10.1111/dmcn.13118...
).

Gestational age may interfere with the development of memory skills and, consequently, language development. Verbal short-term memory is associated with receptive language skills, while expressive skills are associated with working memory(1616 Riva V, Cantiani C, Dionne G, Marini A, Mascheretti S, Molteni M, et al. Working memory mediates the effects of gestational age at birth on expressive language development in children. Neuropsychology. 2017;31(5):475-85. http://dx.doi.org/10.1037/neu0000376. PMid:28383969.
http://dx.doi.org/10.1037/neu0000376...
). In this study, working memory and receptive language skills were not verified, so it is not possible to determine if these relationships would be replicated.

As shown in the literature, changes in memory skills, including short-term verbal skills, may cause difficulties in language development, both comprehension and expression, at different levels(1616 Riva V, Cantiani C, Dionne G, Marini A, Mascheretti S, Molteni M, et al. Working memory mediates the effects of gestational age at birth on expressive language development in children. Neuropsychology. 2017;31(5):475-85. http://dx.doi.org/10.1037/neu0000376. PMid:28383969.
http://dx.doi.org/10.1037/neu0000376...
) and may even lead to impairments for the lexical enlargement during school.

Brazilian researchers(2828 Goto MMF, Gonçalves VMG, Netto AA, Morcillo AM, Moura-Ribeiro MVL. Neurodesenvolvimento de lactentes nascidos a termo pequenos para a idade gestacional no segundo mês de vida. Arq Neuropsiquiatr. 2005;63(1):75-82. http://dx.doi.org/10.1590/S0004-282X2005000100014. PMid:15830069.
http://dx.doi.org/10.1590/S0004-282X2005...
) demonstrated that at two months of life it is already possible to identify risk for neurodevelopmental changes when comparing SGA to AGA infants. SGA infants may be at greater risk for mild abnormalities in neuronal development, cognitive, behavioral, and academic changes(2828 Goto MMF, Gonçalves VMG, Netto AA, Morcillo AM, Moura-Ribeiro MVL. Neurodesenvolvimento de lactentes nascidos a termo pequenos para a idade gestacional no segundo mês de vida. Arq Neuropsiquiatr. 2005;63(1):75-82. http://dx.doi.org/10.1590/S0004-282X2005000100014. PMid:15830069.
http://dx.doi.org/10.1590/S0004-282X2005...
). As shown by our results, 66.7% of SGA infants had difficulties with verbal short-term memory ability. Nevertheless, in this study, no difference was observed between the performance of SGA and AGA infants in this ability, nor in expressive vocabulary, which may suggest that SGA infants may overcome impairments observed at the beginning of development, in the absence of neurological changes and conditions adequate postnatal care.

Our study suggests that the relationship between prematurity, cognitive, and language development is complex. Even when finding similar vocabulary test performance between the groups, it is not possible to state that the language development of premature children will not be affected, because, according to the literature, impairments in verbal short-term memory can negatively impact lexical development(1717 Baddeley A. Working memory. Curr Biol. 2010;20(4):R136-40. http://dx.doi.org/10.1016/j.cub.2009.12.014. PMid:20178752.
http://dx.doi.org/10.1016/j.cub.2009.12....

18 Vugs B, Knoors H, Cuperus J, Hendriks M, Verhoeven L. Interactions between working memory and language in young children with Specific Language Impairment (SLI). Child Neuropsychol. 2015;22(8):1-24. PMid:26144244.

19 Montgomery JW, Magimairaj BM, Finney MC. Working memory and specific language impairment: an update on the relation and perspectives on assessment and treatment. Am J Speech Lang Pathol. 2010;19(1):78-94. http://dx.doi.org/10.1044/1058-0360(2009/09-0028). PMid:19948760.
http://dx.doi.org/10.1044/1058-0360(2009...
-2020 Engel de Abreu PMJ, Gathercole SE, Martin R. Disentangling the relationship between working memory and language: the roles of short-term storage and cognitive control. Learn Individ Differ. 2011;21(5):569-74. http://dx.doi.org/10.1016/j.lindif.2011.06.002.
http://dx.doi.org/10.1016/j.lindif.2011....
).

As mentioned earlier, environmental factors such as language stimulation from the school environment and maternal education may have positively influenced the lexical acquisition of preterm infants, while verbal short-term memory may not have been equally benefited by such factors. Thus, even though premature children did not statistically differ from their term-born peers in lexical ability, the difficulties observed in verbal short-term memory ability, may start to differentiate the groups with increased demand in communicative and educational contexts in the future.

Finally, although there is still no consensus on language impairment in preterm infants, recent studies showed that even children born after 32 weeks of gestation have a higher risk for language disorders than those born at term(2929 Putnick DL, Bornstein MH, Eryigit-Madzwamuse S, Wolke D. Long-term stability of language performance in very preterm, moderate-late preterm, and term children. J Pediatr. 2017;181:74-9. http://dx.doi.org/10.1016/j.jpeds.2016.09.006. PMid:27745750.
http://dx.doi.org/10.1016/j.jpeds.2016.0...
,3030 Sanchez K, Spittle AJ, Cheong JL, Thompson DK, Doyle LW, Anderson PJ, et al. Language in 2-year-old children born preterm and term: a cohort study. Arch Dis Child. 2018;104(7):647-52. PMid:30470685.).

Thus, it would be interesting to continue these investigations, especially performing the longitudinal follow-up of premature children and larger sample size to also measure the impact of environmental factors on their development.

The generalization of the results of this study was limited by the formation of the research group, difficult to obtain due to the low adherence of those responsible and the high rate of absences in the scheduled evaluations, which culminated in a small sample number. Moreover, as it was a cross-sectional study, conducted with a timely assessment of each child, some factors on language development could not be widely explored.

Also, the results presented here show that the lexical development of premature children might occur similarly to typically developing children, indicating the importance of investing in monitoring and early stimulation programs, as well as their insertion in the school environment.

Regarding verbal short-term memory, the difficulties observed in this sample indicated that prematurity might be a biological risk factor for cognitive development, reinforcing the need to follow up premature children in their learning process of language and academic development.

Finally, this study contributes to clinical practice, emphasizing the importance of understanding prematurity as a risk factor for child development and contributes to the debate on the importance of monitoring language development in populations at risk for developing neurodevelopmental disorders.

CONCLUSION

By comparing the performance of children aged 4 to 5 years and 11 months old and a history of prematurity to their term-born peers, we identified that those born prematurely presented similar performance to their peers in vocabulary, but had verbal short term impaired memory.

ACKNOWLEDGEMENTS

To EMEI Monte Castelo for its participation and availability to collect data from the control group. To the Clinical Research Center of the HC-FMUSP Children's Institute, for making the office available for data collection from the research group.

  • Study conducted at the Curso de Fonoaudiologia, Laboratório de Investigação Fonoaudiológica em Desenvolvimento da Linguagem e suas Alterações, Faculdade de Medicina, Universidade de São Paulo – USP; and at the Ambulatório de Seguimento do Recém-nascido de Risco, Centro Neonatal do Instituto da Criança, Instituto da Criança – ICr, Hospital das Clínicas, Faculdade de Medicina, Universidade de São Paulo – USP, – São Paulo (SP), Brasil. Data collection was performed at the Centro de Pesquisa Clínica do Instituto da Criança (ICr), Hospital das Clínicas, Faculdade de Medicina, Universidade de São Paulo, and the Escola Municipal de Educação Infantil Monte Castelo.
  • Financial support: nothing to declare.

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    Montgomery JW, Magimairaj BM, Finney MC. Working memory and specific language impairment: an update on the relation and perspectives on assessment and treatment. Am J Speech Lang Pathol. 2010;19(1):78-94. http://dx.doi.org/10.1044/1058-0360(2009/09-0028) PMid:19948760.
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    » http://dx.doi.org/10.1001/jamapediatrics.2015.2175
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    Taylor CA, Rice ML, Christensen D, Blair E, Zubrick SR. Prenatal and perinatal risks for late language emergence in a population-level sample of twins at age 2. BMC Pediatr. 2018;18(1):41. http://dx.doi.org/10.1186/s12887-018-1035-9 PMid:29415681.
    » http://dx.doi.org/10.1186/s12887-018-1035-9
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    Goto MMF, Gonçalves VMG, Netto AA, Morcillo AM, Moura-Ribeiro MVL. Neurodesenvolvimento de lactentes nascidos a termo pequenos para a idade gestacional no segundo mês de vida. Arq Neuropsiquiatr. 2005;63(1):75-82. http://dx.doi.org/10.1590/S0004-282X2005000100014 PMid:15830069.
    » http://dx.doi.org/10.1590/S0004-282X2005000100014
  • 29
    Putnick DL, Bornstein MH, Eryigit-Madzwamuse S, Wolke D. Long-term stability of language performance in very preterm, moderate-late preterm, and term children. J Pediatr. 2017;181:74-9. http://dx.doi.org/10.1016/j.jpeds.2016.09.006 PMid:27745750.
    » http://dx.doi.org/10.1016/j.jpeds.2016.09.006
  • 30
    Sanchez K, Spittle AJ, Cheong JL, Thompson DK, Doyle LW, Anderson PJ, et al. Language in 2-year-old children born preterm and term: a cohort study. Arch Dis Child. 2018;104(7):647-52. PMid:30470685.

Publication Dates

  • Publication in this collection
    24 Jan 2020
  • Date of issue
    2020

History

  • Received
    07 May 2018
  • Accepted
    25 June 2019
Sociedade Brasileira de Fonoaudiologia Al. Jaú, 684, 7º andar, 01420-002 São Paulo - SP Brasil, Tel./Fax 55 11 - 3873-4211 - São Paulo - SP - Brazil
E-mail: revista@codas.org.br