Sleep in children with microcephaly due to Zika virus infection: a systematic review

Santos, Emanuele Mariano de Souza; Reis, Monique Carla da Silva; Feitosa, Antonio Lucas Ferreira; Medeiros, Andréa Monteiro Correia

doi:10.1590/1980-220X-REEUSP-2020-0507

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REVIEW • Rev. esc. enferm. USP 55 • 2021 • https://doi.org/10.1590/1980-220X-REEUSP-2020-0507 copy

Sleep in children with microcephaly due to Zika virus infection: a systematic review

Sueño en niños con microcefalia debido a la infección por el virus Zika: revisión sistemática

Authorship SCIMAGO INSTITUTIONS RANKINGS

ABSTRACT

Objective:

To review the literature on sleep changes and brain function in children with microcephaly due to Zika virus.

Method:

Systematic review conducted in the databases MEDLINE (PubMed), Scopus, Web of Science, CINAHL, EMBASE, LILACS, and SciELO and the grey databases Google Scholar and OpenGrey.

Results:

Ten Brazilian primary studies with observational research design were included. These were published between 2017 and 2020 with 516 children with microcephaly due to Zika virus infection aged 4 months to 4 years. Out of these, 4 investigated qualitative aspects of sleep using the questionnaires Brief Infant Sleep Questionnaire or Infant Sleep Questionnaire and 6 investigated changes in brain activities during sleep using the Electroencephalogram or Video-Electroencephalogram exams. The children’s quality of sleep was not compromised in most studies. Changes in brain activity during sleep were frequent, with epileptogenic activity being a common finding among the studies.

Conclusion:

The quality of sleep of children with microcephaly due to Zika virus has shown to be similar to that of children with typical development and the presented behavioral changes may be related to changes in electric brain activity.

DESCRIPTORS
Sleep; Microcephaly; Zika Virus Infection; Systematic Review

Database	Strategy	Number of articles
PubMed	(Zika Virus Infection OR ZikV Infection OR Zika Fever OR Zika Virus Disease OR Congenital Zika Syndrome OR Congenital Zika Virus Infection) AND (Sleep OR Sleep Wake Disorders OR Sleep Wake Disorder OR Sleep Disorders OR Sleep Disorder)	20
Scopus	TITLE-ABS-KEY ((zika virus infection OR zikv infection OR zika fever OR zika virus disease OR congenital zika syndrome OR congenital zika virus infection) AND (sleep or sleep wake disorders or sleep wake disorder or sleep disorders or sleep disorder))	4
Web of science	((Zika Virus Infection OR ZikV Infection OR Zika Fever OR Zika Virus Disease OR Congenital Zika Syndrome OR Congenital Zika Virus Infection) AND (Sleep OR Sleep Wake Disorders OR Sleep Wake Disorder OR Sleep Disorders OR Sleep Disorder))	13
CINAHL	(Zika Virus Infection OR ZikV Infection OR Zika Fever OR Zika Virus Disease OR Congenital Zika Syndrome OR Congenital Zika Virus Infection) AND (Sleep OR Sleep Wake Disorders OR Sleep Wake Disorder OR Sleep Disorders OR Sleep Disorder)	36
EMBASE	(‘zika virus infection’/exp OR ‘zika virus infection’ OR (zika AND (‘virus’/exp OR virus) AND (‘infection’/exp OR infection)) OR ‘zikv infection’/exp OR ‘zikv infection’ OR ((‘zikv’/exp OR zikv) AND (‘infection’/exp OR infection)) OR ‘zika fever’/exp OR ‘zika fever’ OR (zika AND (‘fever’/exp OR fever)) OR ‘zika virus disease’ OR (zika AND (‘virus’/exp OR virus) AND (‘disease’/exp OR disease)) OR ‘congenital zika syndrome’/exp OR ‘congenital zika syndrome’ OR ((‘congenital’/exp OR congenital) AND zika AND (‘syndrome’/exp OR syndrome)) OR ‘congenital zika virus infection’ OR ((‘congenital’/exp OR congenital) AND zika AND (‘virus’/exp OR virus) AND (‘infection’/exp OR infection))) AND (‘sleep’/exp OR sleep OR ‘sleep wake disorders’/exp OR ‘sleep wake disorders’ OR ((‘sleep’/exp OR sleep) AND wake AND (‘disorders’/exp OR disorders)) OR ‘sleep wake disorder’/exp OR ‘sleep wake disorder’ OR ((‘sleep’/exp OR sleep) AND wake AND (‘disorder’/exp OR disorder)) OR ‘sleep disorders’/exp OR ‘sleep disorders’ OR ((‘sleep’/exp OR sleep) AND (‘disorders’/exp OR disorders)) OR ‘sleep disorder’/exp OR ‘sleep disorder’ OR ((‘sleep’/exp OR sleep) AND (‘disorder’/exp OR disorder)))	51
LILACS	(Zika Virus Infection OR ZikV Infection OR Zika Fever OR Zika Virus Disease OR Congenital Zika Syndrome OR Congenital Zika Virus Infection)	152
SciELO	(Zika Virus Infection OR ZikV Infection OR Zika Fever OR Zika Virus Disease OR Congenital Zika Syndrome OR Congenital Zika Virus Infection)	220
Google scholar	(Zika Virus Infection OR ZikV Infection OR Zika Fever OR Zika Virus Disease OR Congenital Zika Syndrome OR Congenital Zika Virus Infection) AND (Sleep OR Sleep Wake Disorders OR Sleep Wake Disorder OR Sleep Disorders OR Sleep Disorder)	631
OpenGrey	(Zika Virus Infection OR ZikV Infection OR Zika Fever OR Zika Virus Disease OR Congenital Zika Syndrome OR Congenital Zika Virus Infection) AND (Sleep OR Sleep Wake Disorders OR Sleep Wake Disorder OR Sleep Disorders OR Sleep Disorder)	0

Authors/Year	Design of study	Objective	Sample size and age	Assessment instrument	Results
Wheeler et al., 2018(¹⁷17. Wheeler AC, Ventura CV, Ridenour T, Toth D, Nobrega LL, Dantas LCSS, et al. Skills attained by infants with congenital Zika syndrome: Pilot data from Brazil. PLoS One. 2018;13(7). DOI: http://dx.doi.org/10.1371/journal.pone.0201495. http://dx.doi.org/10.1371/journal.pone.0... )	Cohort	To describe the early development profiles of babies with CZS, focusing on abilities related to solving very early problems, communication, motor and socioemotional development.	Sample: 47 children Age: 13 to 22 months	Brief Infant Sleep Questionnaire (BISQ)	Sleep duration was 9 hours at night, 2.3 hours during the day; sleep latency had a mean of 32 minutes. Sleep problems affected 18%.
Pinato et al., 2018(¹⁸18. Pinato L, Ribeiro EM, Leite RFP, Lopes TF, Pessoa ALS, Guissoni Campos LM, et al. Sleep findings in Brazilian children with congenital Zika syndrome. Sleep. 2018;41(3). DOI: http://dx.doi.org/10.1093/sleep/zsy009. http://dx.doi.org/10.1093/sleep/zsy009... )	Cross-sectional	To investigate the sleep characteristics of 136 babies and young children.	Sample: 88 children with CZS and 38 with typical development (TD) Age: 5 to 24 months, mean of 15.9 months	Brief Infant Sleep Questionnaire (BISQ)	Children with CZS: 34.1% were poor sleepers; 15% stayed awake at night for longer than one hour; 24% slept less than 9 hours. Short total sleeping time, short duration of sleep at night and no correlation between age and being awake at night in relation to TD. 77% had an epilepsy diagnosis.
Lage et al., 2019(¹⁹19. Lage MLC, Carvalho AL, Ventura PA, Taguchi TB, Fernandes AS, Pinho SF, et al. Clinical, neuroimaging, and neurophysiological findings in children with microcephaly related to congenital zika virus infection. Int J Environ Res Public Health. 2019;16(3):309. DOI: http://dx.doi.org/10.3390/ijerph16030309. http://dx.doi.org/10.3390/ijerph16030309... )	Retrospective cross-sectional	To describe the clinical, neurophysiological and neuroradiological characteristics of children with congenital microcephaly diagnosed upon birth and potentially associated to congenital infection with ZikV.	Sample: 102 children Age: mean of 4.1 months VEEG Sample: 96 children	Unspecified standardized assessments VEEG	Irritability/impatient cry in 27.5%, sleep difficulties in 9.8% and epileptogenetic activity in 56.3%.
Kanda et al., 2018(²⁰20. Kanda PAM, Aguiar ADAX, Miranda JL, Falcao AL, Andrade CS, Reis LNDS, et al. Sleep EEG of Microcephaly in Zika Outbreak. Neurodiagn J. 2018;58(1):11-29. DOI: http://dx.doi.org/10.1080/21646821.2018.1428461. http://dx.doi.org/10.1080/21646821.2018.... )	Retrospective cross-sectional	To describe the findings of electroencephalogram (EEG) on the sleep of epileptic children who were born with microcephaly in areas of Brazil with active transmission of Zika virus between 2014 and 2017.	Sample: 23 children Age: 4 to 48 months	EEG	A distinct pattern of EEG was observed in ZikV (5 cases) and rhythmic activity was associated to hypsarrhythmia or slow background, with long periods of rhythmic generalized activity or focal of 4.5 to 24 Hz being common in the EEG of ZikV.
Ferreira et al., 2018(²¹21. Ferreira H, Schiariti V, Regalado I, Sousa K, Pereira S, Fechine C, et al. Functioning and Disability Profile of Children with Microcephaly Associated with Congenital Zika Virus Infection. Int J Environ Res Public Health. 2018;15(6):1107. DOI: http://dx.doi.org/10.3390/ijerph15061107. http://dx.doi.org/10.3390/ijerph15061107... )	Cross-sectional	To describe the functional profile of children with microcephaly associated to ZikV in two states of the Brazilian northeast.	Sample: 34 children Age: mean of 21.2 months	Infant Sleep Questionnaire (ISQ); the results were directly converted into qualifiers of the International Classification of Functioning (ICF).	47.1% reported no disability and 20.6% severe problem in sleep functions (category b134).
Carvalho et al., 2017(²²22. Carvalho MDCG, Miranda-Filho DDB, van der Linden V, Sobral PF, Ramos RCF, Rocha MÂW, et al. Sleep EEG patterns in infants with congenital Zika virus syndrome. Clin Neurophysiol. 2017;128(1):204-14. DOI: http://dx.doi.org/10.1016/j.clinph.2016.11.004. http://dx.doi.org/10.1016/j.clinph.2016.... )	Cohort, case series	To describe the EEG sleep patterns of newborns and children with microcephaly due to congenital Zika virus (ZikV) syndrome.	Sample: 37 children Age: 1 to 5 months	EEG	Different types of EEG abnormalities have been found in CSZ with a predominance of epileptogenic interictal activity and hypsarrhythmia.
Lima, 2017(²³23. Lima DLP. Avaliação do desempenho funcional, do sono e descrição da rede de saúde utilizada por crianças com síndrome congênita do Zika vírus [Dissertation]. Recife: Universidade Federal de Pernambuco; 2017. Available from: https://repositorio.ufpe.br/bitstream/123456789/25094/1/DISSERTA%c3%87%c3%83O%20Danielly%20La%c3%ads%20Pereira%20Lima.pdf. https://repositorio.ufpe.br/bitstream/12... )	Cross-sectional, case series	To assess the functional performance and sleep of children with CSZ between 6 and 18 months of age and describe the health network used by children with CSZ in inland Pernambuco.	Sample: 79 children Age: 6 to 11 months: mean of 10,3 months; 12–18 months: mean of 14.46 months	Brief Infant Sleep Questionnaire (BISQ)	75.9% of the mothers did not consider the sleep of their children a problem. 88,5% of the sample did not awake or awaked only once during sleep at night and 67% slept between 8 and 12 hours per night.
Krueger et al., 2020(²⁴24. Krueger MB, Magalhães SC, Pessoa A, Bueno C, Masruha MR, Sobreira-Neto MA. Electrical status epilepticus during sleep in patients with congenital Zika virus syndrome: An unprecedented clinical finding. Seizure. 2020;81:250-3. DOI: http://dx.doi.org/10.1016/j.seizure.2020.08.019. http://dx.doi.org/10.1016/j.seizure.2020... )	Case series	To assess the clinical and neurophysiological characteristics of patients with congenital Zika virus syndrome who presented a pattern of electric epileptic state during slow-wave sleep (ESES).	Sample: 4 children Age: 4 years	VEEG	Epilepsy diagnosed between one month and 18 months of age, presenting an ESES pattern at three years of age. The children presented a wide range of epileptic symptoms, but all experienced tonic convulsions.
van der Linden et al., 2020(²⁵25. van der Linden H, van der Linden V, Pessoa A, Valente KD. Continuous epileptiform discharges during sleep as an evolutionary pattern in patients with congenital Zika virus syndrome. Epilepsia. 2020;61(9). DOI: http://dx.doi.org/10.1111/epi.16631. http://dx.doi.org/10.1111/epi.16631... )	Longitudinal	To describe the evolutive patterns of EEG after the second year of life in a long series of cases of patients with confirmed CZVS.	Sample: 55 children Age: mean of 50 months	EEG and VEEG	Continuous epileptic discharges during non-rapid eye movement sleep were identified in 40% of the children; in 90.1%, this pattern was symmetrical, with a previous predominance of epilepsy-like activity; with severe epilepsy in 68.2%. Subcortical calcification and multi focal EEGs in previous ages occurred more frequently in patients with this pattern. Other unspecified interictal EEG patterns were epilepsy-like focal discharges in 41.8% and multi-focal activity in 10.9%.
Sequerra et al., 2020(²⁶26. Sequerra EB, Rocha AJ, Medeiros GOC, Neto MM, Maia CRS, Arrais NMR, et al. Association between brain morphology and electrophysiological features in Congenital Zika Virus Syndrome: A cross-sectional, observational study. EClinicalMedicine. 2020;26:100508. DOI: https://doi.org/10.1016/j.eclinm.2020.100508. https://doi.org/10.1016/j.eclinm.2020.10... )	Cross-sectional	To present perceptive correlations between the occurrence of epilepsy-like discharges and rhombencephalon malformation, prosencephalon volume and oscillations related to sleep.	Sample: 47 children Age: unspecified	EEG Computerized tomography	Epilepsy diagnosis for 62% of the sample, with epileptic-like discharges, including interictal unilateral peaks (90%), bilateral synchronous and asynchronous interictal peaks (72%) and hypsarrhythmia (41%). 58% of children with clinical epilepsy were born with rhombencephalon malformations associated to epilepsy. The presence of interictal epileptic-like discharges (IED) was associated to smaller brain volumes. 25% presented sleep spindles associated to the presence of IED.

Author, year	1	2	3	4	5	6	7	8	9	10	11	12	13	14
Wheeler et al., 2018(¹⁵15. Moher D, Liberati A, Tetzlaff J, Altman DG. Preferred Reporting Items for Systematic Reviews and Meta-Analyses: The PRISMA Statement. PLoS Med. 2009;6(7):e1000097. DOI: https://dx.plos.org/10.1371/journal.pmed.1000097. https://dx.plos.org/10.1371/journal.pmed... )	Y	Y	Y	Y	Y	NA	NA	N	Y	N	CD	N	NA	N
Pinato et al., 2018(¹⁶16. Munn Z, Moola S, Lisy K, Riitano D, Tufanaru C. Chapter 5: Systematic reviews of prevalence and incidence. In: Aromataris E, Munn Z (editors). JBI Manual for Evidence Synthesis. JBI, 2020. Available from: https://synthesismanual.jbi.global. DOI: https://doi.org/10.46658/JBIMES-20-06. https://synthesismanual.jbi.global... )	Y	Y	Y	Y	CD	NA	Y	Y	Y	N	NR	N	NA	N
Lage et al., 2019(¹⁷17. Wheeler AC, Ventura CV, Ridenour T, Toth D, Nobrega LL, Dantas LCSS, et al. Skills attained by infants with congenital Zika syndrome: Pilot data from Brazil. PLoS One. 2018;13(7). DOI: http://dx.doi.org/10.1371/journal.pone.0201495. http://dx.doi.org/10.1371/journal.pone.0... )	Y	Y	Y	Y	CD	NA	NA	N	Y	NR	NA	N	NA	NR
Kanda et al., 2018(¹⁸18. Pinato L, Ribeiro EM, Leite RFP, Lopes TF, Pessoa ALS, Guissoni Campos LM, et al. Sleep findings in Brazilian children with congenital Zika syndrome. Sleep. 2018;41(3). DOI: http://dx.doi.org/10.1093/sleep/zsy009. http://dx.doi.org/10.1093/sleep/zsy009... )	Y	Y	Y	Y	CD	NA	NA	Y	Y	N	N	N	NA	NR
Ferreira et al., 2018(¹⁹19. Lage MLC, Carvalho AL, Ventura PA, Taguchi TB, Fernandes AS, Pinho SF, et al. Clinical, neuroimaging, and neurophysiological findings in children with microcephaly related to congenital zika virus infection. Int J Environ Res Public Health. 2019;16(3):309. DOI: http://dx.doi.org/10.3390/ijerph16030309. http://dx.doi.org/10.3390/ijerph16030309... )	Y	Y	CD	Y	CD	NA	Y	N	Y	N	Y	N	NA	CD
Carvalho et al., 2017(²⁰20. Kanda PAM, Aguiar ADAX, Miranda JL, Falcao AL, Andrade CS, Reis LNDS, et al. Sleep EEG of Microcephaly in Zika Outbreak. Neurodiagn J. 2018;58(1):11-29. DOI: http://dx.doi.org/10.1080/21646821.2018.1428461. http://dx.doi.org/10.1080/21646821.2018.... )	Y	Y	Y	Y	CD	N	Y	N	Y	N	N	N	NA	NR
Lima, 2017(²¹21. Ferreira H, Schiariti V, Regalado I, Sousa K, Pereira S, Fechine C, et al. Functioning and Disability Profile of Children with Microcephaly Associated with Congenital Zika Virus Infection. Int J Environ Res Public Health. 2018;15(6):1107. DOI: http://dx.doi.org/10.3390/ijerph15061107. http://dx.doi.org/10.3390/ijerph15061107... )	Y	Y	Y	Y	Y	NA	Y	N	Y	N	Y	N	NA	CD
Krueger et al., 2020(²²22. Carvalho MDCG, Miranda-Filho DDB, van der Linden V, Sobral PF, Ramos RCF, Rocha MÂW, et al. Sleep EEG patterns in infants with congenital Zika virus syndrome. Clin Neurophysiol. 2017;128(1):204-14. DOI: http://dx.doi.org/10.1016/j.clinph.2016.11.004. http://dx.doi.org/10.1016/j.clinph.2016.... )	Y	Y	NR	Y	Y	Y	Y	N	N	N	N	N	N	NR
van der Linden et al., 2020(²³23. Lima DLP. Avaliação do desempenho funcional, do sono e descrição da rede de saúde utilizada por crianças com síndrome congênita do Zika vírus [Dissertation]. Recife: Universidade Federal de Pernambuco; 2017. Available from: https://repositorio.ufpe.br/bitstream/123456789/25094/1/DISSERTA%c3%87%c3%83O%20Danielly%20La%c3%ads%20Pereira%20Lima.pdf. https://repositorio.ufpe.br/bitstream/12... )	Y	Y	Y	NR	Y	Y	Y	N	N	N	N	N	N	N
Sequerra et al., 2020(²⁴24. Krueger MB, Magalhães SC, Pessoa A, Bueno C, Masruha MR, Sobreira-Neto MA. Electrical status epilepticus during sleep in patients with congenital Zika virus syndrome: An unprecedented clinical finding. Seizure. 2020;81:250-3. DOI: http://dx.doi.org/10.1016/j.seizure.2020.08.019. http://dx.doi.org/10.1016/j.seizure.2020... )	Y	Y	Y	Y	Y	Y	Y	Y	N	N	N	N	N	NR

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[1] Corresponding author: Emanuele Mariano de Souza Santos, Rua Doutor Jorge de Lima 113, Trapiche da Barra, 57010-382 – Maceió, AL, Brazil, manumsouza@yahoo.com.br