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      Functioning and Disability Profile of Children with Microcephaly Associated with Congenital Zika Virus Infection

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          Abstract

          Introduction: The increase in the number of cases of microcephaly in Brazil and its association with the Zika virus (ZIKV) is a global public health problem. The International Classification of Functioning Disability and Health (ICF) model is a powerful tool and extremely relevant in managing disability. Objective: Describe the functioning profile of children with microcephaly associated with ZIKV in two states of northeastern Brazil. Methods: This is a descriptive cross-sectional study. The sociodemographic characteristics, head circumference, and other clinical data were collected from medical charts, physical examinations, measuring instruments, and interviews with the children and their parents. The Brazilian Portuguese version of the Brief Common ICF Core Set for cerebral palsy (CP) was used. Each ICF category was assigned a qualifier, which ranged from 0 to 4 (no problem, mild problem, moderate problem, severe problem, complete problem). For environmental factors, 0 represents no barrier and 4 represents complete barrier; +0, no facilitator and +4, complete facilitator. Results: A total of 34 children with microcephaly caused by ZIKV were recruited (18 girls and 16 boys) at four rehabilitation facilities in Rio Grande do Norte and Paraíba states, Brazil. The average age of the participants was 21 months, monthly income was ≈USD 300.00, and head circumference z-scores ranged between 0.92 and −5.51. The functioning profile revealed complete disability in most of the body function categories (b). The activity and participation areas (d) were highly impacted, particularly in mobility-related categories. With respect to environmental factors (e), most of the sample reported a complete facilitator for the immediate family, friends, and health services, systems, and policies, as well as a complete barrier to societal attitudes. Conclusion: This is the first study that describes the functioning profile of children with microcephaly associated with ZIKV, using a tool based on the ICF in Brazil. Our findings reinforce the need to maximize health care and access to information, based on the ICF, for multiprofessional teams, administrators, family members, and children.

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          Most cited references 41

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          Description of 13 Infants Born During October 2015-January 2016 With Congenital Zika Virus Infection Without Microcephaly at Birth - Brazil.

          Congenital Zika virus infection can cause microcephaly and severe brain abnormalities (1). Congenital Zika syndrome comprises a spectrum of clinical features (2); however, as is the case with most newly recognized teratogens, the earliest documented clinical presentation is expected to be the most severe. Initial descriptions of the effects of in utero Zika virus infection centered prominently on the finding of congenital microcephaly (3). To assess the possibility of clinical presentations that do not include congenital microcephaly, a retrospective assessment of 13 infants from the Brazilian states of Pernambuco and Ceará with normal head size at birth and laboratory evidence of congenital Zika virus infection was conducted. All infants had brain abnormalities on neuroimaging consistent with congenital Zika syndrome, including decreased brain volume, ventriculomegaly, subcortical calcifications, and cortical malformations. The earliest evaluation occurred on the second day of life. Among all infants, head growth was documented to have decelerated as early as 5 months of age, and 11 infants had microcephaly. These findings provide evidence that among infants with prenatal exposure to Zika virus, the absence of microcephaly at birth does not exclude congenital Zika virus infection or the presence of Zika-related brain and other abnormalities. These findings support the recommendation for comprehensive medical and developmental follow-up of infants exposed to Zika virus prenatally. Early neuroimaging might identify brain abnormalities related to congenital Zika infection even among infants with a normal head circumference (4).
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            Early Growth and Neurologic Outcomes of Infants with Probable Congenital Zika Virus Syndrome

            We report the early growth and neurologic findings of 48 infants in Brazil diagnosed with probable congenital Zika virus syndrome and followed to age 1–8 months. Most of these infants had microcephaly (86.7%) and craniofacial disproportion (95.8%). The clinical pattern included poor head growth with increasingly negative z-scores, pyramidal/extrapyramidal symptoms, and epilepsy.
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              Health and Development at Age 19–24 Months of 19 Children Who Were Born with Microcephaly and Laboratory Evidence of Congenital Zika Virus Infection During the 2015 Zika Virus Outbreak — Brazil, 2017

              In November 2015, the Brazilian Ministry of Health (MOH) declared the Zika virus outbreak a public health emergency after an increase in microcephaly cases was reported in the northeast region of the country ( 1 ). During 2015–2016, 15 states in Brazil with laboratory-confirmed Zika virus transmission reported an increase in birth prevalence of microcephaly (2.8 cases per 10,000 live births), significantly exceeding prevalence in four states without confirmed transmission (0.6 per 10,000) ( 2 ). Although children with microcephaly and laboratory evidence of Zika virus infection have been described in early infancy ( 3 ), their subsequent health and development have not been well characterized, constraining planning for the care and support of these children and their families. The Brazilian MOH, the State Health Secretariat of Paraíba, and CDC collaborated on a follow-up investigation of the health and development of children in northeastern Brazil who were reported to national surveillance with microcephaly at birth. Nineteen children with microcephaly at birth and laboratory evidence of Zika virus infection were assessed through clinical evaluations, caregiver interviews, and review of medical records. At follow-up (ages 19–24 months), most of these children had severe motor impairment, seizure disorders, hearing and vision abnormalities, and sleep difficulties. Children with microcephaly and laboratory evidence of Zika virus infection have severe functional limitations and will require specialized care from clinicians and caregivers as they age. The Zika Outcomes and Development in Infants and Children (ZODIAC) investigation sought to compile a comprehensive description of health and development among children aged >12 months who were born with microcephaly and participated in a 2016 case-control investigation. The case-control investigation assessed the association of Zika virus infection and microcephaly among children aged 1–7 months, living in Paraíba state. The children and their caregivers were evaluated by multidisciplinary teams at two state clinics in Campina Grande and João Pessoa (macroregions 1 and 2) in Paraíba state during August–October 2017. This report describes a subsample of 19 children, aged 19–24 months, who participated in ZODIAC and were born with microcephaly and with laboratory evidence of Zika virus infection. All children in the ZODIAC investigation were born from October 1, 2015 through January 31, 2016, and were reported to the Registro de Eventos de Saúde Pública (RESP)—Microcefalias, Brazil’s national microcephaly registry. For infants to be eligible for the 2016 case-control investigation, their mothers must have resided in Paraíba state for at least 80% of their pregnancy. For the ZODIAC investigation, microcephaly was defined as head circumference below the third percentile for gestational age and sex, according to INTERGROWTH 21st standards ( 4 ). Subsequent measurements are reported in standard deviations (SD) to better characterize growth deficiencies ( 5 ). Laboratory evidence of Zika virus infection was defined as a positive test for Zika virus immunoglobulin M (IgM) and virus specific-neutralizing antibodies or a positive test for Zika virus-specific neutralizing antibodies in an infant sample ( 6 ). Samples were obtained at age 1–7 months in the 2016 case-control investigation, and any evidence of infection was assumed to be prenatal in origin. Results of prenatal and newborn testing to rule out other congenital infections were available for some infants and their mothers. ZODIAC data were collected through clinical evaluations, caregiver interviews, and review of medical records. Licensed physicians performed growth, ophthalmologic and physical exams, and a neurologic assessment. Physicians were trained to use the Hammersmith Infant Neurological Examination (HINE), a standardized neurologic exam, to assess neuromotor function and visual and auditory responses ( 7 ). Trained interviewers administered screening and assessment instruments to the primary caregiver (usually the mother) regarding the child’s health and development, including a seizure screener ( 8 ), the Ages and Stages Questionnaires (ASQ-3),* and the Ages and Stages Social-Emotional Questionnaires (ASQ:SE). † Data were captured in REDCap, a secure web application. The families of 278 previously studied children residing in the ZODIAC investigation catchment area were eligible for inclusion; 122 children were enrolled, including 19 who were aged 3 SDs below the mean for their age and sex. TABLE 1 Growth measurements* of children aged 19–24 months with confirmed or probable congenital Zika virus infection†,§ and microcephaly classification at birth¶,** — Paraíba, Brazil, August–October 2017 Growth No. (%) Male (n = 10) Female (n = 9) Head circumference†† >3 SD below mean for age and sex§§ 7 (70) 8 (89) Length¶¶ 1–3 SD below mean for age and sex*** 6 (60) 7 (78) Weight††† 1 to >3 SD below mean for age and sex§§§ 6 (60) 7 (78) Abbreviation: SD = standard deviation. * http://www.who.int/childgrowth/standards/en . † Confirmed congenital Zika virus infection was indicated by a positive Zika virus-specific immunoglobulin M [IgM] capture enzyme-linked immunosorbent assay [MAC-ELISA] result on infant cerebrospinal fluid [CSF] or serum) and positive plaque reduction neutralization testing (PRNT). Serologic evidence without confirmation via PRNT indicated probable congenital Zika virus infection. § http://jcm.asm.org/content/38/5/1823.full.pdf+html. ¶ Microcephaly at birth was defined according to the internationally accepted definition, head circumference below the 3rd percentile for gestational age and sex, from the standards for newborns and references for very preterm infants compiled by the International Fetal and Newborn Growth Consortium for the 21st Century. ** https://intergrowth21.tghn.org/ . †† http://www.who.int/childgrowth/standards/hc_for_age/en/ . §§ Of the remaining males, three (30%) had a head circumference equal to the mean or up to 1 SD below the mean, and of the remaining females, one (11%) had a head circumference equal to the mean or up to 1 SD above the mean. ¶¶ http://www.who.int/childgrowth/standards/height_for_age/en/. *** Of the remaining males, the length of 4 (40%) was equal to the mean or up to 3 SDs above the mean, and of the remaining females, the length of 2 (22%) was equal to the mean or up to 1 SD above the mean. ††† http://www.who.int/childgrowth/standards/weight_for_age/en/. §§§ Of the remaining males, the weight of 3 (30%) was equal to the mean or up to 2 SDs above the mean; the weight of 1 (10%) male was >3 SDs above the mean. Of the remaining females, the weight of 2 (22%) was equal to the mean or up to 2 SDs above the mean. TABLE 2 Growth parameters,* evaluations, and medical and developmental conditions for 19 infants aged 19–24 months with confirmed or probable congenital Zika virus infection,†,§ and microcephaly classification¶,** at birth — ZODIAC investigation, Paraíba, Brazil, August–October 2017 Infant no. Sex Birth HC** (%) ZODIAC HC†† (Z score) ZODIAC weight§§ (Z score) Brain imaging consistent with CZS Zika laboratory evidence Seizures Eating challenges Sleep challenges Severe motor impairment Vision limitation Hearing abnormalities ASQ-3 age interval¶¶ 1 F 6 months 17 M 6 months 18 F 6 months 19 M 6 months Abbreviations: ASQ-3 = Ages and Stages-III Questionnaire; CZS = congenital Zika syndrome; F = female; HC = head circumference; IgM = immunoglobulin M; M = male; NAb = neutralizing antibodies; ZODIAC = Zika Outcomes and Development in Infants and Children. * http://www.who.int/childgrowth/standards/en . † Confirmed congenital Zika virus infection was indicated by a positive Zika virus-specific IgM capture enzyme-linked immunosorbent assay result on infant cerebrospinal fluid or serum) and positive plaque reduction neutralization testing (PRNT). Serologic evidence without confirmation via PRNT indicated probable congenital Zika virus infection. § http://jcm.asm.org/content/38/5/1823.full.pdf+html. ¶ Microcephaly at birth was defined according to the internationally accepted definition, head circumference below the 3rd percentile for gestational age and sex from the standards for newborns and references for very preterm infants compiled by the International Fetal and Newborn Growth Consortium for the 21st Century. ** https://intergrowth21.tghn.org/ . †† http://www.who.int/childgrowth/standards/hc_for_age/en/ . §§ http://www.who.int/childgrowth/standards/weight_for_age/en/. ¶¶ The ASQ-3 is a series of 21 parent-completed questionnaires designed to screen the developmental performance of children aged 1–66 months in the areas of communication, gross motor skills, fine motor skills, problem solving, and personal-social skills (http://agesandstages.com); based on ASQ-3 screening, an age interval of <6 months indicates that the child’s parent-reported developmental progress has not advanced beyond that typical of an infant at age 6 months. Eleven children screened positive for nonfebrile seizures, indicating possible seizure disorder (Table 2) (Table 3). Caregivers reported that eight children were previously hospitalized, including six hospitalized for bronchitis/pneumonia, and that 10 children had frequent sleeping difficulties and nine had eating or swallowing challenges. Thirteen children had an impaired response to auditory stimuli. Four children had retinal abnormalities and 11 had an impaired response to visual stimuli. Fifteen children did not pass the ASQ-3 age interval questionnaire designed for a child aged 6 months. Fifteen children had a global score below 40 on the HINE, indicating severe motor impairment, including 14 who had findings consistent with cerebral palsy ( 7 ). Outcomes including feeding challenges, sleeping difficulties, severe motor impairment, vision and hearing abnormalities, and seizures tended to co-occur. All children had at least one of these outcomes, 12 had three to five of these outcomes, and two had all six outcomes. Four children (infant number 16, 17, 18, and 19) (Table 2) had typical growth and development at follow-up and might have been misclassified at birth. TABLE 3 Health and developmental outcomes of 19 children aged 19–24 months with confirmed or probable congenital Zika virus infection,* ,† and microcephaly classification§,¶ at birth — Paraíba, Brazil, August–October 2017 Outcome No. (%) Medical findings Seizures**,†† 11 (58) Retinal abnormalities§§ 4 (21) Hospitalization** 8 (42) Pneumonia/Bronchitis 6 (75) Intestinal infection 1 (14) High fever 1 (14) Failure to thrive/feed 1 (14) Functional outcomes Sleeping difficulties** 10 (53) Feeding difficulties** 9 (47) Impaired response to auditory stimuli (hearing asymmetric or no response)¶¶ 13 (68) Impaired response to visual stimuli¶¶ 11 (58) Neurologic outcomes¶¶ Severe motor impairment¶¶ 15 (79) Cerebral palsy*** 14 (74) * Confirmed congenital Zika virus infection was indicated by a positive Zika virus-specific immunoglobulin M capture enzyme-linked immunosorbent assay result on infant cerebrospinal fluid or serum and positive plaque reduction neutralization testing (PRNT) at birth. Serologic evidence without confirmation via PRNT indicated probable congenital Zika virus infection. † http://jcm.asm.org/content/38/5/1823.full.pdf+html. § Microcephaly at birth was defined according to the internationally accepted definition, head circumference below the 3rd percentile for gestational age and sex from the standards for newborns and references for very preterm infants compiled by the International Fetal and Newborn Growth Consortium for the 21st Century. ¶ https://intergrowth21.tghn.org/. ** Reported by the caregiver. †† https://doi.org/10.1016/j.pediatrneurol.2015.09.016 . §§ Retinal abnormalities were identified by ophthalmologic exam. ¶¶ Motor function, functional hearing, and functional vision were assessed using the Hammersmith Infant Neurologic Exam (HINE). A global score below 40 on the HINE is associated with severe motor impairment, according to findings published in 2016 (https://doi.org/10.1111/dmcn.12876). *** Cerebral palsy was identified by neurologist. Discussion As of September 2017, 2,986 newborns with microcephaly in Brazil were reported to RESP and 2,959 cases are being monitored ( 9 ). Children with Zika virus–associated microcephaly face medical and functional challenges that span many areas of development. Previous reports established a baseline of poor health outcomes at birth, including severe brain and ophthalmologic abnormalities, and other serious central nervous system abnormalities ( 3 ). This report expands on initial findings by demonstrating that specific outcomes, such as severe motor impairment and impaired visual and auditory response to stimuli, affect the majority of children with evidence of congenital Zika virus infection and microcephaly and become more apparent as these children age. Approximately three quarters of young children affected by Zika virus infection in this analysis had at least three of the specified co-occurring outcomes. Many of the initial findings identified at birth remain present at ages 19–24 months, and these children are falling far behind in achievement of age-appropriate developmental milestones, indicating the need for long-term follow-up and support. The findings in this report are subject to at least four limitations. First, although all children with microcephaly recruited into the 2016 case-control investigation from selected areas of Paraíba state were offered enrollment in the ZODIAC investigation, not all families chose to participate. Consequently, the findings might not be representative of all children with microcephaly associated with congenital Zika virus infection. Second, errors in head circumference measurement at birth and passive transfer of maternal antibodies might have led to misidentification and might explain the divergent observations for the four children showing more typical development. Additionally, some of the parent-assessment findings, such as those from the seizure screener, were not medically verified. Finally, the ages of infants in the original case-control investigation ranged from 1 to 7 months at the time of blood collection, and it is possible that the laboratory results for some infants reflected postnatal, rather than prenatal, exposure. This report provides information on the ongoing challenges facing children with severe congenital Zika virus syndrome; these children will require specialized care from clinicians and caregivers as they age. These findings allow for anticipation of medical and social service needs of affected children and their families, including early intervention services, and planning for resources to support these families in health care and community settings in Brazil, the United States, and other countries. Children with disabilities related to congenital Zika virus infection will need multidisciplinary care from various pediatric subspecialists ( 10 ). Long-term follow-up and measurement of developmental progression of children affected by Zika virus can inform intervention services and sub-specialties needed to provide optimal care for these children. Summary What is already known about this topic? Congenital Zika virus infection has been linked to increased rates of microcephaly and a unique pattern of birth defects among infants. Although children with microcephaly and laboratory evidence of Zika virus infection have been described in early infancy, the subsequent health and development in young children have not been well characterized, constraining planning for the care of these children. What is added by this report? The growth and development of 19 children, aged 19–24 months, with laboratory evidence of Zika virus infection were thoroughly assessed. All children had at least one adverse outcome including feeding challenges, sleeping difficulties, severe motor impairment, vision and hearing abnormalities, and seizures, and these outcomes tended to co-occur. What are the implications for public health practice? Children with microcephaly and laboratory evidence of Zika virus infection face medical and functional challenges that span many areas of development, some of which become more evident as children age. They will continue to require specialized care from clinicians and caregivers. These data allow for anticipation of medical and social services needs of affected children and families, such as early intervention services, and planning for resources to support these families in healthcare and community settings.
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                Author and article information

                Journal
                Int J Environ Res Public Health
                Int J Environ Res Public Health
                ijerph
                International Journal of Environmental Research and Public Health
                MDPI
                1661-7827
                1660-4601
                29 May 2018
                June 2018
                : 15
                : 6
                Affiliations
                [1 ]Postgraduate Program in Collective Health, Federal University of Rio Grande do Norte—Faculty of Health Sciences of Trairi (UFRN-FACISA), Santa Cruz 59200-000, Brazil; haryelle_naryma@ 123456yahoo.com.br (H.N.C.F.); galante@ 123456facisa.ufrn.br (K.G.S.); apsilvana@ 123456gmail.com (S.A.P.)
                [2 ]Division of Medical Sciences, University of Victoria, BC V8W 2Y2, Canada; vschiariti@ 123456cw.bc.ca
                [3 ]Postgraduate Program in Physical Therapy, Federal University of Rio Grande do Norte, Natal 59078-970, Brazil; isabellyrodrigues_@ 123456hotmail.com
                [4 ]Undegraduate Program in Physical Therapy, UNIPÊ, João Pessoa 58053-000, Brazil; carla.novaes@ 123456unipe.br
                Author notes
                [* ]Correspondence: egmarlongo@ 123456yahoo.es ; Tel.: +55-84-32912411
                Article
                ijerph-15-01107
                10.3390/ijerph15061107
                6025082
                29844290
                © 2018 by the authors.

                Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license ( http://creativecommons.org/licenses/by/4.0/).

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                Public health

                icf, public health, zika virus infection, microcephaly, children

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