{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,21]],"date-time":"2026-08-21T12:17:33Z","timestamp":1787314653156,"version":"build-2736575974"},"reference-count":34,"publisher":"MDPI AG","issue":"7","license":[{"start":{"date-parts":[[2024,6,22]],"date-time":"2024-06-22T00:00:00Z","timestamp":1719014400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Coordena\u00e7\u00e3o de Aperfei\u00e7oamento de Pessoal de N\u00edvel Superior\u2014Brasil","award":["001"],"award-info":[{"award-number":["001"]}]},{"name":"Coordena\u00e7\u00e3o de Aperfei\u00e7oamento de Pessoal de N\u00edvel Superior\u2014Brasil","award":["16\/2024"],"award-info":[{"award-number":["16\/2024"]}]},{"name":"Coordena\u00e7\u00e3o de Aperfei\u00e7oamento de Pessoal de N\u00edvel Superior\u2014Brasil","award":["312322\/2022-4"],"award-info":[{"award-number":["312322\/2022-4"]}]},{"name":"Coordena\u00e7\u00e3o de Aperfei\u00e7oamento de Pessoal de N\u00edvel Superior\u2014Brasil","award":["316762\/2021-0"],"award-info":[{"award-number":["316762\/2021-0"]}]},{"name":"Pr\u00f3-Reitoria de P\u00f3s-Gradua\u00e7\u00e3o\/Unesp EDITAL PROPG","award":["001"],"award-info":[{"award-number":["001"]}]},{"name":"Pr\u00f3-Reitoria de P\u00f3s-Gradua\u00e7\u00e3o\/Unesp EDITAL PROPG","award":["16\/2024"],"award-info":[{"award-number":["16\/2024"]}]},{"name":"Pr\u00f3-Reitoria de P\u00f3s-Gradua\u00e7\u00e3o\/Unesp EDITAL PROPG","award":["312322\/2022-4"],"award-info":[{"award-number":["312322\/2022-4"]}]},{"name":"Pr\u00f3-Reitoria de P\u00f3s-Gradua\u00e7\u00e3o\/Unesp EDITAL PROPG","award":["316762\/2021-0"],"award-info":[{"award-number":["316762\/2021-0"]}]},{"name":"National Council for Scientific and Technological Development","award":["001"],"award-info":[{"award-number":["001"]}]},{"name":"National Council for Scientific and Technological Development","award":["16\/2024"],"award-info":[{"award-number":["16\/2024"]}]},{"name":"National Council for Scientific and Technological Development","award":["312322\/2022-4"],"award-info":[{"award-number":["312322\/2022-4"]}]},{"name":"National Council for Scientific and Technological Development","award":["316762\/2021-0"],"award-info":[{"award-number":["316762\/2021-0"]}]},{"name":"National Council for Scientific and Technological Development","award":["001"],"award-info":[{"award-number":["001"]}]},{"name":"National Council for Scientific and Technological Development","award":["16\/2024"],"award-info":[{"award-number":["16\/2024"]}]},{"name":"National Council for Scientific and Technological Development","award":["312322\/2022-4"],"award-info":[{"award-number":["312322\/2022-4"]}]},{"name":"National Council for Scientific and Technological Development","award":["316762\/2021-0"],"award-info":[{"award-number":["316762\/2021-0"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Viruses"],"abstract":"<jats:p>AIM: Congenital Zika Virus Syndrome (CZS) presents notable hurdles to neurodevelopment, with language development emerging as a crucial aspect. This study investigates sleep patterns and language skills in children with CZS, aiming to explore the potential synchronization of sleep development with their neurodevelopment. METHOD: We studied cross-sectionally 135 children with CZS aged 0 to 48 months, investigating sleep using the BISQ Questionnaire. Language development was assessed using the Early Language Milestone Scale, while motor development and cognitive and social ability were assessed using the Bayley Scales of Infant and Young Child Development 3rd edition. We also studied longitudinally a cohort of 16 children (initially aged 0 to 12 months) whom we followed for four years, assessing at one-year intervals. RESULTS: Sleep disturbances and language deficits were highly frequent in this population. In the 0\u201312 months group, a late bedtime and frequent nighttime awakenings were associated with poorer auditory expressive skills. At 13\u201324 months, nighttime awakenings were associated with poorer auditory expressive skills, while among 25\u201336-month-olds decreased auditory receptive skills were associated with longer sleep onset latency and reduced nighttime sleep duration. CONCLUSION: The brain alterations caused by Zika virus infection affect both sleep disturbances and delays in language development. It is possible that sleep disturbance may be a mediating factor in the pathway between CZS and delayed language development, as the three analyzed language skills showed a correlation with sleep parameters.<\/jats:p>","DOI":"10.3390\/v16071003","type":"journal-article","created":{"date-parts":[[2024,6,24]],"date-time":"2024-06-24T03:53:43Z","timestamp":1719201223000},"page":"1003","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":6,"title":["Association between Sleep and Language Development in Children with Congenital Zika Syndrome"],"prefix":"10.3390","volume":"16","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-8828-9854","authenticated-orcid":false,"given":"Nathani C.","family":"da Silva","sequence":"first","affiliation":[{"name":"Department of Speech, Language and Hearing Sciences, S\u00e3o Paulo State University (UNESP), Mar\u00edlia 17525-900, Brazil"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Celia M.","family":"Giacheti","sequence":"additional","affiliation":[{"name":"Department of Speech, Language and Hearing Sciences, S\u00e3o Paulo State University (UNESP), Mar\u00edlia 17525-900, Brazil"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Maria C. H. do","family":"Couto","sequence":"additional","affiliation":[{"name":"Department of Speech, Language and Hearing Sciences, S\u00e3o Paulo State University (UNESP), Mar\u00edlia 17525-900, Brazil"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Stefany S.","family":"de Jesus","sequence":"additional","affiliation":[{"name":"Department of Speech, Language and Hearing Sciences, S\u00e3o Paulo State University (UNESP), Mar\u00edlia 17525-900, Brazil"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Erlane M.","family":"Ribeiro","sequence":"additional","affiliation":[{"name":"Albert Sabin Children\u2019s Hospital, Fortaleza 60410-790, Brazil"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Islane M. C.","family":"Ver\u00e7osa","sequence":"additional","affiliation":[{"name":"Center for Perfecting Sight See Hope Reviver (CAVIVER), Fortaleza 60110-370, Brazil"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Luciana","family":"Pinato","sequence":"additional","affiliation":[{"name":"Department of Speech, Language and Hearing Sciences, S\u00e3o Paulo State University (UNESP), Mar\u00edlia 17525-900, Brazil"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2024,6,22]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"2099","DOI":"10.1016\/S0140-6736(17)31450-2","article-title":"An update on Zika virus infection","volume":"390","author":"Baud","year":"2017","journal-title":"Lancet"},{"key":"ref_2","first-page":"e00069018","article-title":"The microcephaly epidemic and Zika virus: Building knowledge in epidemiology","volume":"34","author":"Albuquerque","year":"2018","journal-title":"Cad. Saude Publica"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"288","DOI":"10.1001\/jamapediatrics.2016.3982","article-title":"Characterizing The Pattern Of Anomalies In Congenital Zika Syndrome For Pediatric Clinicians","volume":"171","author":"Moore","year":"2017","journal-title":"Jama Pediatr."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"zsy009","DOI":"10.1093\/sleep\/zsy009","article-title":"Sleep findings in Brazilian children with congenital Zika syndrome","volume":"41","author":"Pinato","year":"2018","journal-title":"Sleep"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"378","DOI":"10.1016\/S2352-4642(20)30041-9","article-title":"Neurological outcomes of congenital Zika syndrome in toddlers and preschoolers: A case series","volume":"4","author":"Pereira","year":"2020","journal-title":"Lancet Child. Adolesc. Health"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"537","DOI":"10.1177\/0883073820983163","article-title":"Complications and sequelae in patients with congenital microcephaly associated with zika virus infection: Two-year follow-up","volume":"36","author":"Gouvea","year":"2021","journal-title":"J. Child Neurol."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"314","DOI":"10.1590\/0100-3984.2017.0098","article-title":"Congenital Zika syndrome and neuroimaging findings: What do we know so far?","volume":"50","author":"Ribeiro","year":"2017","journal-title":"Radiol. Bras."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"227","DOI":"10.3389\/fneur.2018.00227","article-title":"Nervous System Injury and Neuroimaging of Zika Virus Infection","volume":"9","author":"Wu","year":"2018","journal-title":"Front. Neurol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"1427","DOI":"10.3174\/ajnr.A5216","article-title":"Nonmicrocephalic infants with congenital Zika syndrome suspected only after neuroimaging evaluation compared with those with microcephaly at birth and postnatally: How large is the Zika virus \u201ciceberg\u201d?","volume":"38","author":"Aragao","year":"2017","journal-title":"AJNR. Am. J. Neuroradiol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"14","DOI":"10.1016\/j.seizure.2020.11.004","article-title":"Epilepsy after congenital zika virus infection: EEG and neuroimaging features","volume":"84","author":"Nunes","year":"2021","journal-title":"Seizure"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"101719","DOI":"10.1016\/j.infbeh.2022.101719","article-title":"Infant sleep and development: Concurrent and longitudinal relations during the first 8 months of life","volume":"67","author":"Pecora","year":"2022","journal-title":"Infant. Behav. Dev."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"103549","DOI":"10.1016\/j.ridd.2019.103549","article-title":"Sleep is atypical across neurodevelopmental disorders in infants and toddlers: A cross-syndrome study","volume":"97","author":"Plunkett","year":"2020","journal-title":"Res. Dev. Disabil."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"427","DOI":"10.1038\/nn.4479","article-title":"REM sleep selectively prunes and maintains new synapses in development and learning","volume":"20","author":"Li","year":"2017","journal-title":"Nat. Neurosci."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"366","DOI":"10.3389\/fpsyt.2019.00366","article-title":"Systematic Review of Sleep Disturbances and Circadian Sleep Desynchronization in Autism Spectrum Disorder: Toward an Integrative Model of a Self-Reinforcing Loop","volume":"10","author":"Carmassi","year":"2019","journal-title":"Front. Psychiatry"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"60","DOI":"10.1111\/j.1365-2214.2012.01412.x","article-title":"Psychosocial and somatic outcomes of sleep problems in children: A 4-year follow-up study","volume":"40","author":"Simola","year":"2014","journal-title":"Child. Care Health Dev."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"347","DOI":"10.3389\/fnhum.2015.00347","article-title":"Influence of sleep disorders on the behavior of individuals with autism spectrum disorder","volume":"9","author":"Fadini","year":"2015","journal-title":"Front. Hum. Neurosci."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"105842","DOI":"10.1016\/j.earlhumdev.2023.105842","article-title":"Language skills development in children with congenital Zika virus syndrome","volume":"184","author":"Pinato","year":"2023","journal-title":"Early Hum. Dev."},{"key":"ref_18","first-page":"89","article-title":"de la P.R.; Sadeh, A. BISQ Questionnaire for Infant Sleep Assessment: Translation into brazilian portuguese","volume":"5","author":"Nunes","year":"2012","journal-title":"Sleep Sci."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"1549","DOI":"10.5664\/jcsm.6288","article-title":"Consensus Statement of the American Academy of Sleep Medicine on the Recommended Amount of Sleep for Healthy Children: Methodology and Discussion","volume":"12","author":"Paruthi","year":"2016","journal-title":"J. Clin. Sleep Med."},{"key":"ref_20","unstructured":"Coplan, J. (1993). Early Language Milestone Scale, ProEd Inc.. [2nd ed.]."},{"key":"ref_21","first-page":"189","article-title":"Bayley-III Scales of Infant and Toddler Development: Transcultural Adaptation and Psychometric Properties","volume":"26","author":"Madaschi","year":"2016","journal-title":"Paid. Ribeir\u00e3o Preto"},{"key":"ref_22","unstructured":"(2024, March 16). How Much Sleep Do Babies and Kids Need?. Available online: https:\/\/www.sleepfoundation.org\/children-and-sleep\/how-much-sleep-do-kids-need#:~:text=Newborns%20typically%20sleep%2016%20to,hours%20of%20sleep%20each%20day."},{"key":"ref_23","first-page":"955","article-title":"Brain circuitry controlling sleep and wakefulness","volume":"23","author":"Horner","year":"2017","journal-title":"Continuum"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"e12715","DOI":"10.1111\/jpi.12715","article-title":"Disrupted nocturnal melatonin in autism: Association with tumor necrosis factor and sleep disturbances","volume":"70","author":"Fadini","year":"2021","journal-title":"J. Pineal Res."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"1344","DOI":"10.1111\/dmcn.14920","article-title":"Sleep problems in children with cerebral palsy and their parents","volume":"63","author":"Hulst","year":"2021","journal-title":"Dev. Med. Child Neurol."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"93","DOI":"10.1016\/j.smrv.2017.10.007","article-title":"Benefits of a bedtime routine in young children: Sleep, development, and beyond","volume":"40","author":"Mindell","year":"2018","journal-title":"Sleep Med. Rev."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"135","DOI":"10.2147\/NSS.S125992","article-title":"Infant sleep and its relation with cognition and growth: A narrative review","volume":"9","author":"Tham","year":"2017","journal-title":"Nat. Sci. Sleep"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"90","DOI":"10.1016\/j.sleep.2017.03.009","article-title":"Auditory behavior and auditory temporal resolution in children with sleep-disordered breathing","volume":"34","author":"Silva","year":"2017","journal-title":"Sleep Med."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"503","DOI":"10.1111\/jsr.12306","article-title":"Napping facilitates word learning in early lexical development","volume":"24","author":"Myers","year":"2015","journal-title":"J. Sleep Res."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"345","DOI":"10.1097\/YCO.0000000000000790","article-title":"Children with neurodevelopmental disorders: How do they sleep?","volume":"35","author":"Belli","year":"2022","journal-title":"Curr. Opin. Psychiatry"},{"key":"ref_31","doi-asserted-by":"crossref","unstructured":"Li, Q.K.W., MacKinnon, A.L., Tough, S., Graham, S., and Tomfohr-Madsen, L. (2022). Does Where You Live Predict What You Say? Associations between Neighborhood Factors, Child Sleep, and Language Development. Brain Sci., 12.","DOI":"10.3390\/brainsci12020223"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"122","DOI":"10.1007\/s12519-022-00647-w","article-title":"Childhood sleep: Physical, cognitive, and behavioral consequences and implications","volume":"20","author":"Liu","year":"2022","journal-title":"World J. Pediatr."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"205","DOI":"10.1016\/S0896-6273(02)00746-8","article-title":"Practice with sleep makes perfect: Sleep-dependent motor skill learning","volume":"35","author":"Walker","year":"2002","journal-title":"Neuron"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"557","DOI":"10.1016\/j.neuroscience.2004.05.053","article-title":"Sleep and rest facilitate auditory learning","volume":"127","author":"Gottselig","year":"2004","journal-title":"Neuroscience"}],"container-title":["Viruses"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1999-4915\/16\/7\/1003\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T15:02:48Z","timestamp":1760108568000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1999-4915\/16\/7\/1003"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,6,22]]},"references-count":34,"journal-issue":{"issue":"7","published-online":{"date-parts":[[2024,7]]}},"alternative-id":["v16071003"],"URL":"https:\/\/doi.org\/10.3390\/v16071003","relation":{},"ISSN":["1999-4915"],"issn-type":[{"value":"1999-4915","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,6,22]]}}}