Sex influences on the neurocognitive outcome of preterm children.


Journal

Journal of neuroscience research
ISSN: 1097-4547
Titre abrégé: J Neurosci Res
Pays: United States
ID NLM: 7600111

Informations de publication

Date de publication:
05 2023
Historique:
revised: 06 05 2021
received: 15 01 2021
accepted: 07 05 2021
medline: 4 4 2023
pubmed: 17 6 2021
entrez: 16 6 2021
Statut: ppublish

Résumé

This article presents a revision of the literature regarding the influence of sex differences on the recovery and long-term behavioral and cognitive outcomes of preterm children. After initial discussion of some methodological concerns, the literature regarding the concept of "male disadvantage," which is often used when talking about early neurological and psychomotor outcomes in preterm children, is presented. Subsequently, the literature data on sex-related differences in preterm children are discussed, focusing on their influence on the developmental pathways of cognition, language, executive function, behavior and affect, and response to rehabilitation therapies. Finally, evidence about brain structural and connectivity correlates of sex differences in the brain of preterm survivors is taken into account. Although visuo-spatial and visuo-perceptual functioning is widely studied in the preterm child and is strongly sex specific, little to no data are available regarding male-female differences in preterm children and the interaction effect between sex and preterm birth. For this reason, original data analyses of male-female differences in visuo-spatial performance from a small sample of preterm children are also presented.

Identifiants

pubmed: 34133788
doi: 10.1002/jnr.24862
doi:

Types de publication

Journal Article Review

Langues

eng

Sous-ensembles de citation

IM

Pagination

796-811

Informations de copyright

© 2021 Wiley Periodicals, LLC.

Références

Allen, L., Leon-Attia, O., Shaham, M., Shefer, S., & Gabis, L. V. (2020). Autism risk linked to prematurity is more accentuated in girls. PLoS ONE, 15(8), e0236994. https://doi.org/10.1371/journal.pone.0236994
Ask, H., Gustavson, K., Ystrom, E., Havdahl, K. A., Tesli, M., Askeland, R. B., & Reichborn-Kjennerud, T. (2018). Association of gestational age at birth with symptoms of attention-deficit/hyperactivity disorder in children. JAMA Pediatrics, 172(8), 749-756. https://doi.org/10.1001/jamapediatrics.2018.1315
Atkinson, J., & Braddick, O. (2007). Visual and visuocognitive development in children born very prematurely. Progress in Brain Research, 164, 123-149.
Atkinson, J., Braddick, O., Rose, F. E., Searcy, Y. M., Wattam-Bell, J., & Bellugi, U. (2006). Dorsal-stream motion processing deficits persist into adulthood in williams syndrome. Neuropsychologia, 44(5), 828-833. https://doi.org/10.1016/j.neuropsychologia.2005.08.002
Benassi, M., Bolzani, R., Forsman, L., Ådén, U., Jacobson, L., Giovagnoli, S., & Hellgren, K. (2018). Motion perception and form discrimination in extremely preterm school-Aged children. Child Development, 89(6), e494-e506.
Broström, L., Vollmer, B., Bolk, J., Eklöf, E., & Ådén, U. (2018). Minor neurological dysfunction and associations with motor function, general cognitive abilities, and behaviour in children born extremely preterm. Developmental Medicine & Child Neurology, 60(8), 826-832. https://doi.org/10.1111/dmcn.13738
CDC. (2014). Prevalence of autism spectrum disorder among children aged 8 years-Autism and developmental disabilities monitoring network, 11 sites, United States, 2010. MMWR Surveillance Summaries, 63(2), 1-21.
Doyle, L. W., Cheong, J. L. Y., Burnett, A., Roberts, G., Lee, K. J., & Anderson, P. J., & Victorian Infant Collaborative Study Group. (2015). Biological and social influences on outcomes of extreme-preterm/low-birth weight adolescents. Pediatrics, 136(6), e1513-e1520. https://doi.org/10.1542/peds.2015-2006
Duerden, E. G., Card, D., Lax, I. D., Donner, E. J., & Taylor, M. J. (2013). Alterations in frontostriatal pathways in children born very preterm. Developmental Medicine & Child Neurology, 55(10), 952-958. https://doi.org/10.1111/dmcn.12198
Elgen, S. K., Sommerfelt, K., Leversen, K. T., & Markestad, T. (2015). Minor neurodevelopmental impairments are associated with increased occurrence of ADHD symptoms in children born extremely preterm. European Child & Adolescent Psychiatry, 24(4), 463-470. https://doi.org/10.1007/s00787-014-0597-9
Engle, W. A. (2004). Age terminology during the perinatal period. Pediatrics, 114(5), 1362-1364.
Ferrari, F. (Ed.). (2017). Il neonato pretermine. Disordini dello sviluppo e interventi precoci. Fondazione Pierfranco e Luisa Mariani. Franco Angeli.
Fevang, S. K., Hysing, M., Markestad, T., & Sommerfelt, K. (2016). Mental health in children born extremely preterm without severe neurodevelopmental disabilities. Pediatrics, 137(4), e20153002. https://doi.org/10.1542/peds.2015-3002
Gabis, L. V., Hacham-Pilosof, K., Yosef, O. B., Rabinovitz, G., Leshem, G., Shilon-Hadass, A., Biran, Y., Reichman, B., Kuint, J., & Bart, O. (2015). The influence of a multisensory intervention for preterm infants provided by parents, on developmental abilities and on parental stress levels. Journal of Child Neurology, 30(7), 896-903. https://doi.org/10.1177/0883073814549242
Garfinkle, J., Yoon, E. W., Alvaro, R., Nwaesei, C., Claveau, M., Lee, S. K., & Investigators, C. N. N. (2020). Trends in sex-specific differences in outcomes in extreme preterms: Progress or natural barriers? Archives of Disease in Childhood - Fetal and Neonatal Edition, 105(2), 158-163. https://doi.org/10.1136/archdischild-2018-316399
Glass, H. C., Costarino, A. T., Stayer, S. A., Brett, C. M., Cladis, F., & Davis, P. J. (2015). Outcomes for extremely premature infants. Anesthesia and Analgesia, 120(6), 1337-1351. https://doi.org/10.1213/ANE.0000000000000705
Guzzetta, A., Tinelli, F., Del Viva, M. M., Bancale, A., Arrighi, R., Pascale, R. R., & Cioni, G. (2009). Motion perception in preterm children: Role of prematurity and brain damage. NeuroReport, 20(15), 1339-1343. https://doi.org/10.1097/WNR.0b013e328330b6f3
Hack, M., Friedman, H., & Fanaroff, A. A. (1996). Outcomes of extremely low birth weight infants. Pediatrics, 98(5), 931-937.
Hintz, S. R., Kendrick, D. E., Vohr, B. R., Poole, W. K., Higgins, R. D. & Nichd Neonatal Research Network. (2006). Gender differences in neurodevelopmental outcomes among extremely preterm, extremely low birthweight infants. Acta Paediatrica, 95(10), 1239-1248. https://doi.org/10.1080/08035250600599727
Johnson, S., Kochhar, P., Hennessy, E., Marlow, N., Wolke, D., & Hollis, C. (2016). Antecedents of attention-deficit/hyperactivity disorder symptoms in children born extremely preterm. Journal of Developmental and Behavioral Pediatrics, 37(4), 285-297. https://doi.org/10.1097/DBP.0000000000000298
Joseph, R. M., O'Shea, T. M., Allred, E. N., Heeren, T., Hirtz, D., Paneth, N., Leviton, A., & Kuban, K. C. K. (2017). Prevalence and associated features of autism spectrum disorder in extremely low gestational age newborns at age 10 years. Autism Research, 10(2), 224-232. https://doi.org/10.1002/aur.1644
Kozhemiako, N., Nunes, A. S., Vakorin, V. A., Chau, C. M. Y., Moiseev, A., Ribary, U., Grunau, R. E., & Doesburg, S. M. (2020). Sex differences in brain connectivity and male vulnerability in very preterm children. Human Brain Mapping, 41(2), 388-400. https://doi.org/10.1002/hbm.24809
Kumar, P., Shankaran, S., Ambalavanan, N., Kendrick, D. E., Pappas, A., Vohr, B. R., Poindexter, B. B., Das, A., & Higgins, R. D. (2013). Characteristics of extremely low-birth-weight infant survivors with unimpaired outcomes at 30 months of age. Journal of Perinatology, 33(10), 800-805. https://doi.org/10.1038/jp.2013.71
Limperopoulos, C., Chilingaryan, G., Sullivan, N., Guizard, N., Robertson, R. L., & Du Plessis, A. J. (2014). Injury to the premature cerebellum: Outcome is related to remote cortical development. Cerebral Cortex, 24(3), 728-736. https://doi.org/10.1093/cercor/bhs354
Limperopoulos, C., Soul, J. S., Haidar, H., Huppi, P. S., Bassan, H., Warfield, S. K., & du Plessis, A. J. (2005). Impaired trophic interactions between the cerebellum and the cerebrum among preterm infants. Pediatrics, 116(4), 844-850.
Linsell, L., Malouf, R., Morris, J., Kurinczuk, J. J., & Marlow, N. (2015). Prognostic factors for poor cognitive development in children born very preterm or with very low birth weight: A systematic review. JAMA Pediatrics, 169(12), 1162-1172. https://doi.org/10.1001/jamapediatrics.2015.2175
Macedo, I., Pereira-da-Silva, L., Brito, L., & Cardoso, M. (2019). Male sex is an independent risk factor for poor neurodevelopmental outcome at 20 months corrected age, in human milk-fed very preterm infants: A cohort study. Einstein, 17(3), eAO4607. https://doi.org/10.31744/einstein_journal/2019AO4607
Månsson, J., Fellman, V., Stjernqvist, K., & EXPRESS Study Group (authors). (2015). Extremely preterm birth affects boys more and socio-economic and neonatal variables pose sex-specific risks. Acta Paediatrica, 104(5), 514-521. https://doi.org/10.1111/apa.12937
Milner, A. D. (2017). How do the two visual streams interact with each other? Experimental Brain Research, 235(5), 1297-1308. https://doi.org/10.1007/s00221-017-4917-4
Miyake, A., Friedman, N. P., Emerson, M. J., Witzki, A. H., Howerter, A., & Wager, T. D. (2000). The unity and diversity of executive functions and their contributions to complex frontal lobe tasks: A latent variable analysis. Cognitive Psychology, 41(1), 49-100. https://doi.org/10.1006/cogp.1999.0734
Naeye, R. L., Burt, L. S., Wright, D. L., Blanc, W. A., & Tatter, D. (1971). Neonatal mortality, the male disadvantage. Pediatrics, 48(6), 902-906.
Olsen, I. E., Groveman, S. A., Lawson, M. L., Clark, R. H., & Zemel, B. S. (2010). New intrauterine growth curves based on united states data. Pediatrics, 125(2), e214-e224. https://doi.org/10.1542/peds.2009-0913
Pavlova, M., Staudt, M., Sokolov, A., Birbaumer, N., & Krägeloh-Mann, I. (2003). Perception and production of biological movement in patients with early periventricular brain lesions. Brain, 126(3), 692-701. https://doi.org/10.1093/brain/awg062
Romeo, D. M., Brogna, C., Sini, F., Romeo, M. G., Cota, F., & Ricci, D. (2016). Early psychomotor development of low-risk preterm infants: Influence of gestational age and gender. European Journal of Paediatric Neurology, 20(4), 518-523. https://doi.org/10.1016/j.ejpn.2016.04.011
Romeo, D. M., Guzzardi, S., Ricci, D., Cilauro, S., Brogna, C., Cowan, F., Romeo, M. G., & Mercuri, E. (2012). Longitudinal cognitive assessment in healthy late preterm infants. European Journal of Paediatric Neurology, 16(3), 243-247. https://doi.org/10.1016/j.ejpn.2011.07.012
Saigal, S., & Doyle, L. W. (2008). An overview of mortality and sequelae of preterm birth from infancy to adulthood. Lancet, 371(9608), 261-269.
Sanchez, K., Spittle, A. J., Cheong, J. L., Thompson, D. K., Doyle, L. W., Anderson, P. J., & Morgan, A. T. (2019). Language in 2-year-old children born preterm and term: A cohort study. Archives of Disease in Childhood, 104(7), 647-652. https://doi.org/10.1136/archdischild-2018-315843
Sansavini, A., Guarini, A., Savini, S., Broccoli, S., Justice, L., Alessandroni, R., & Faldella, G. (2011). Longitudinal trajectories of gestural and linguistic abilities in very preterm infants in the second year of life. Neuropsychologia, 49(13), 3677-3688. https://doi.org/10.1016/j.neuropsychologia.2011.09.023
Schmidt, B., Whyte, R. K., Asztalos, E. V., Moddemann, D., Poets, C., Rabi, Y., Solimano, A., Roberts, R. S., & Canadian Oxygen Trial (COT) Group. (2013). Effects of targeting higher vs lower arterial oxygen saturations on death or disability in extremely preterm infants: A randomized clinical trial. JAMA, 309(20), 2111-2120. https://doi.org/10.1001/jama.2013.5555
Sellier, E., Platt, M. J., Andersen, G. L., Krägeloh-Mann, I., De La Cruz, J., Cans, C., & Chalmers, J. (2016). Decreasing prevalence in cerebral palsy: A multi-site European population-based study, 1980 to 2003. Developmental Medicine & Child Neurology, 58(1), 85-92. https://doi.org/10.1111/dmcn.12865
Shim, S., Cho, S. J., Kong, K. A., & Park, E. A. (2017). Gestational age-specific sex difference in mortality and morbidities of preterm infants: A nationwide study. Scientific Reports, 7(1), 1-8. https://doi.org/10.1038/s41598-017-06490-8
Skiöld, B., Alexandrou, G., Padilla, N., Blennow, M., Vollmer, B., & Ådén, U. (2014). Sex differences in outcome and associations with neonatal brain morphology in extremely preterm children. Journal of Pediatrics, 164(5), 1012-1018. https://doi.org/10.1016/j.jpeds.2013.12.051
Spong, C. Y. (2013). Defining “term” pregnancy: Recommendations from the defining “Term” pregnancy workgroup. JAMA, 309(23), 2445-2446. https://doi.org/10.1001/jama.2013.6235
Stenson, B. J., Tarnow-Mordi, W. O., Darlow, B. A., Simes, J., Juszczak, E., Askie, L., & Cairns, P. (2013). Oxygen saturation and outcomes in preterm infants. New England Journal of Medicine, 368(22), 2094-2104.
Tinelli, F., Bulgheroni, S., Mazzotti, S., Vago, C., Groppo, M., Scaramuzzo, R. T., Riva, D., & Cioni, G. (2014). Ventral stream sensitivity in “healthy” preterm-born adolescents: Psychophysical and neuropsychological evaluation. Early Human Development, 90(1), 45-49. https://doi.org/10.1016/j.earlhumdev.2013.10.006
Tyson, J. E., Parikh, N. A., Langer, J., Green, C., & Higgins, R. D. (2008). Intensive care for extreme prematurity-Moving beyond gestational age. New England Journal of Medicine, 358(16), 1672-1681. https://doi.org/10.1056/NEJMoa073059
van Houdt, C. A., Oosterlaan, J., van Wassenaer-Leemhuis, A. G., van Kaam, A. H., & Aarnoudse-Moens, C. S. (2019). Executive function deficits in children born preterm or at low birthweight: A meta-analysis. Developmental Medicine & Child Neurology, 61(9), 1015-1024. https://doi.org/10.1111/dmcn.14213
Vaucher, Y. E., Peralta-Carcelen, M., Finer, N. N., Carlo, W. A., Gantz, M. G., Walsh, M. C., Laptook, A. R., Yoder, B. A., Faix, R. G., Das, A., Schibler, K., Rich, W., Newman, N. S., Vohr, B. R., Yolton, K., Heyne, R. J., Wilson-Costello, D. E., Evans, P. W., Goldstein, R. F., … Higgins, R. D. (2012). Neurodevelopmental outcomes in the early CPAP and pulse oximetry trial. New England Journal of Medicine, 367(26), 2495-2504. https://doi.org/10.1056/NEJMoa1208506
Villamor-Martinez, E., Fumagalli, M., Alomar, Y. I., Passera, S., Cavallaro, G., Mosca, F., & Villamor, E. (2019). Cerebellar hemorrhage in preterm infants: A meta-analysis on risk factors and neurodevelopmental outcome. Frontiers in Physiology, 10, 800. https://doi.org/10.3389/fphys.2019.00800
Vu, H. D., Dickinson, C., & Kandasamy, Y. (2018). Sex difference in mortality for premature and low birth weight neonates: A systematic review. American Journal of Perinatology, 35(08), 707-715. https://doi.org/10.1055/s-0037-1608876
Warrington, E. K., & James, M. (1991). The visual object and space perception battery. Pearson Assessment.
World Health Organization. (2012). Born too soon: The global action report on preterm birth. Author.
World Health Organization. (2013). March of dimes; the partnership for maternal newborn & child health. Author.
Yaari, M., Mankuta, D., Harel- Gadassi, A., Friedlander, E., Bar-Oz, B., Eventov-Friedman, S., Maniv, N., Zucker, D., & Yirmiya, N. (2018). Early developmental trajectories of preterm infants. Research in Developmental Disabilities, 81, 12-23. https://doi.org/10.1016/j.ridd.2017.10.018

Auteurs

Matilde Taddei (M)

Developmental Neurology Unit, Fondazione IRCCS Istituto Neurologico Carlo Besta, Milan, Italy.

Francesca Tinelli (F)

Department of Developmental Neuroscience, IRCCS Fondazione Stella Maris, Calambrone, Italy.

Flavia Faccio (F)

Developmental Neurology Unit, Fondazione IRCCS Istituto Neurologico Carlo Besta, Milan, Italy.

Daria Riva (D)

Developmental Neurology Unit, Fondazione IRCCS Istituto Neurologico Carlo Besta, Milan, Italy.

Sara Bulgheroni (S)

Developmental Neurology Unit, Fondazione IRCCS Istituto Neurologico Carlo Besta, Milan, Italy.

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