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Article

Clinical and Acoustic Alterations of Swallowing in Children Exposed to Zika Virus during Pregnancy in a Cohort in Amazonas, Brazil: A Case Series Study

by
Cristina de Souza Rodrigues
1,
Raillon Keven Santos Souza
2,
Cosmo Vieira Rocha Neto
3,
Rodrigo Haruo Otani
3,
Daniel de Medeiros Batista
3,
Ana Karla Nelson de Oliveira Maia
3,
Kleber Pinheiro de Oliveira Filho
4,
Thais Dourado de Andrade
4,
Emmilyn de Andrade Almeida
5,
Luiz Henrique Gonçalves Maciel
1,
Lucíola de Fátima Albuquerque Almeida Peixoto Castro
1,
Marília Rosa Abtibol-Bernardino
1,6,
Djane Clarys Baia-da-Silva
1,3,4,7,*,
Silvana Gomes Benzecry
3,
Marcia da Costa Castilho
8,
Flor Ernestina Martínez-Espinosa
1,7,8,
Maria das Graças Costa Alecrim
1,9,
Rosane Sampaio Santos
10 and
Camila Botto-Menezes
1,3,8,*
1
Postgraduate Program in Tropical Medicine (PPGMT), University of Amazonas State (UEA), Manaus 69040-000, Brazil
2
Northern University Center (UniNorte), Manaus 69020-160, Brazil
3
School of Health Sciences, University of Amazonas State, Manaus 69065-001, Brazil
4
Faculty of Pharmacy, University Nilton Lins, Manaus 69058-030, Brazil
5
East Zone Children’s Emergency Hospital, Manaus 69058-030, Brazil
6
Department of Maternal and Child Health, Medical School, Federal University of Amazonas, Manaus 69020-160, Brazil
7
Leônidas & Maria Deane Institute, Fiocruz Amazonia, Manaus 69057-070, Brazil
8
Tropical Medicine Foundation Doutor Heitor Vieira Dourado (FMT-HVD), Manaus 69040-000, Brazil
9
Medical Course Coordination at Manaus Metropolitan College/FAMETRO, Manaus 69050-000, Brazil
10
Postgraduate Program in Communication Disorders (PPGDIC), University of Tuiuti do Paraná (UTP), Paraná 82010-210, Brazil
*
Authors to whom correspondence should be addressed.
Viruses 2023, 15(12), 2363; https://doi.org/10.3390/v15122363
Submission received: 15 September 2023 / Revised: 13 November 2023 / Accepted: 13 November 2023 / Published: 30 November 2023
(This article belongs to the Special Issue Zika Virus and Congenital Zika Syndrome)
Versions Notes

Abstract

:
Oropharyngeal dysphagia (OD) is a swallowing disorder that involves difficulty in safely passing the food bolus from the oral cavity to the stomach. OD is a common problem in children with congenital Zika virus syndrome (CZS). In this case series, we describe the clinical and acoustic alterations of swallowing in children exposed to the Zika virus during pregnancy in a cohort from Amazonas, Brazil. From July 2019 to January 2020, 22 children were evaluated, 6 with microcephaly and 16 without microcephaly. The mean age among the participants was 35 months (±4.6 months). All children with microcephaly had alterations in oral motricity, mainly in the lips and cheeks. Other alterations were in vocal quality, hard palate, and soft palate. Half of the children with microcephaly showed changes in cervical auscultation during breast milk swallowing. In children without microcephaly, the most frequently observed alteration was in lip motricity, but alterations in auscultation during the swallowing of breast milk were not observed. Regarding swallowing food of a liquid and pasty consistency, the most frequent alterations were incomplete verbal closure, increased oral transit time, inadequacy in capturing the spoon, anterior labial leakage, and increased oral transit time. Although these events are more frequent in microcephalic children, they can also be seen in non-microcephalic children, which points to the need for an indistinct evaluation of children exposed in utero to ZIKV.

1. Introduction

Zika virus (ZIKV) is a flavivirus arbovirus transmitted primarily through the bite of female Aedes mosquitoes [1]. It was first identified in Uganda, Africa, in 1947, with its first epidemic occurring on Yap Island in Micronesia; however, there have been previous reports of infection in humans in other countries in Africa and Asia [2,3,4]. ZIKV was identified in the Americas, more specifically in Brazil, at the end of 2015, although phylogenetic studies have identified the arrival to have been in mid-2013 [5,6,7]. In Brazil, the high number of cases of microcephaly in children exposed in utero to ZIKV in 2015 evidenced the important association and the need for multidisciplinary follow-up of pregnant women exposed to ZIKV and their children [8,9,10]. ZIKV infection during pregnancy, especially in the first and second trimesters of pregnancy, can trigger damage to the fetus’s central nervous system, especially during embryonic development, resulting in impactful characteristics for the child [11,12]. The main implications of intrauterine exposure are complications from congenital Zika virus syndrome (CZVS), changes in growth and development, and low birth weight, in addition to speech and swallowing problems [13,14,15,16,17,18,19].
Oral and phonological impairments are associated with microcephaly induced by ZIKV and include bruxism, mixed breathing, changes in muscle tone that compromise the swallowing process, hearing loss, dysphagia, altered tongue frenulum, and delays in neuropsychomotor and language development [19,20,21,22,23,24,25]. Oropharyngeal dysphagia (OD) is a swallowing disorder that involves difficulty in safely passing the food bolus from the oral cavity to the esophagus [26,27]. OD can be caused by neurological factors arising from congenital abnormalities or combined with damage associated with diseases of the oral cavity, pharynx, and upper esophageal sphincter [28,29]. OD can lead to complications such as aspiration pneumonia, dehydration, and malnutrition associated with inadequate nutritional intake [30]. Among the typical signs and symptoms of OD are dysfunction of the labial or facial muscles, inability to chew or push food, xerostomia, sialorrhea, difficulty in initiating swallowing, nasal regurgitation, the need for several swallows, coughing, and wet voice during and after meals [30,31,32]. It is necessary to identify which phase or which phases of swallowing are compromised (oral, pharyngeal, or esophageal phases), as well as the etiology (stroke, head injury, dementia, Parkinson’s disease, cancer, multiple sclerosis, myasthenia gravis, dermatomyositis, complicated reflux, or large hiatal hernias) and degree of dysphagia (mild, moderate, or severe) [29,33].
In ZIKV-related dysphagia, mostly associated with microcephaly, the child has difficulty in managing liquid consistency, due to changes in facial muscles, decreased muscle tone, and intraoral hyposensitivity, which causes oral leakage through the labial commissures and silent aspiration [34,35]. This study describes the clinical and acoustic characteristics of the swallowing of children exposed to ZIKV during pregnancy and cared for in a tertiary unit, to serve as a reference for the diagnosis and treatment of tropical and infectious diseases in the Amazon.

2. Materials and Methods

Children born between March 2016 and June 2018 from mothers studied in previous cohorts [17,36,37] were clinically evaluable in terms of their swallowing ability. Mothers’ information was obtained from electronic medical records. The ZIKV infection in the mother was confirmed in a blood or urine sample through real-time reverse transcriptase polymerase chain reaction (RT-PCR) detection. RT-PCR was performed following the protocol of Lanciotti et al. [38] at the Central Public Health Laboratory in Amazonas (LACEN-AM). Tests for Dengue-virus, Parvovirus-B19-virus infections, and the detection of etiological agents of TORCH Syndrome and malaria were performed by the Virology Laboratory and Clinical Analysis Laboratory at the Tropical Medicine Foundation Doutor Heitor Vieira Dourado (FMT-HVD), as previously described [17]. These infections were evaluated because they can induce embryonic malformations.
The clinical and laboratory variables of the children during birth are summarized in Table 1. The children’s eating habits were obtained through interviews with the parents. Children were not evaluated for ZIKV infection. The clinical assessment was performed using the pediatric dysphagia clinical evaluation protocol 2014 (PAD-PED) [39]. The development of the stomatognathic system was carried out according to the previously described methodology [40]. Posture, tone/strength, structure, and/or motility of the lips, tongue, cheek, and palate were evaluated (Table 2). Vocal quality, mucosa aspect, frequency of saliva swallowing, and cervical auscultation were also evaluated. Swallowing in the oral and pharyngeal phases was primarily assessed using foods provided by the Nutrition Department of the FMT-HVD, and the selection of consistencies respected the participant’s food introduction (Table 3). All clinical and swallowing assessments were performed by an experienced speech therapist.
The acoustic analysis of swallowing was performed using a portable Doppler sonar (DS) device (wave angle sound: 3 MHz). This equipment was coupled to the notebook software and the acoustic sounds were recorded and later analyzed using Deglutisom software® version 2018.02.07. The transducer was positioned on the right side of the neck, in the lateral portion of the trachea, just below the cricoid cartilage. To reduce dispersion and advance the sound recording, conductive gel was used. The instrument used to collect acoustic information was the Acoustic Swallowing Assessment Protocol (PAAD) [41]. OD was defined as an alteration in the clinical evaluation of structural and functional features, evaluation of saliva swallowing, evaluation of non-nutritive sucking, and evaluation with food, and/or the presence of alterations in the acoustic signs of swallowing.
OD was defined and classified based on PAD-PED and Oliveira et al.’s work [40], as absent (no abnormalities), mild (presence of impaired oropharyngeal transit, but without signs of aspiration), moderate (i.e., impaired oropharyngeal transit, with the presence of aspiration signs and preserved protection mechanisms, allowing clearance of the lower airways), and serious (i.e., compromised oropharyngeal transit, with signs suggestive of aspiration and an absence of protective mechanisms).
This study was approved by the FMT-HVD Research Ethics Committee, being assigned ethical approval number 08941019.2.0000.0005/2019. All guardians of the participants provided formal written consent. The variables of interest in this study were registered in a standardized questionnaire using Epi Info software, version 7. Data analyses were carried out in the Stata program, version 13. The results were expressed through relative frequencies, with mean and standard deviation.

3. Results

Table 1 expresses the baseline characteristics of children exposed to ZIKV infection in the intrauterine period in Manaus, Amazonas, Brazil. From July 2019 to January 2020, 22 children were evaluated, 6 with microcephaly (cases 4, 6, 7, 8, 15, and 19) during the assessment and 17 without microcephaly. Five children were microcephalic at birth (cases 4, 6, 8, 15, and 19). In other words, case 7 is classified as postnatal microcephaly, although the mother had a confirmed ZIKV infection. The neurological characteristics of three microcephalic children are described in Supplementary Table S1 (cases 4, 7, and 19). The mean gestational and enrollment ages were 38.9 weeks (±0.86 weeks) and 35 months (±4.6 months), respectively. The children averaged 2.99 kg (±0.44 kg) at birth. The neonatal hearing screening was not suitable for one child, while the tongue test was altered for one child (7.1%, case 1). Cardiac and/or respiratory problems were seen in three children (cases 4, 5, and 11). No mother tested positive for Dengue-virus, Parvovirus-B19-virus infections, etiological agents of TORCH Syndrome, or malaria during the pregnancy.
Changes in oral motricity and the frequency of saliva swallowing through structural and functional evaluation are shown in Table 2. All children with microcephaly presented alterations in oral motricity, mainly in the lips and cheeks (100%, 6/6), hard palate (cases 6, 7, and 8), soft palate (cases 6, 8, and 15), and vocal quality (cases 7, 8, 15, and 19). In children without microcephaly, the most frequently observed alteration was in lip motricity, seen in 43.7% (7/16). In both groups, the appearance of the oral mucosa was adequate (100%, 22/22). In terms of the frequency of saliva swallowing, children with microcephaly mostly had sialorrhea (50%, cases 6, 8, and 19) and sialostasis (33.3%, cases 7 and 15). In terms of cervical auscultation, 50% of the children with microcephaly (cases 8, 15, and 19) had alterations after swallowing. In conclusion, three cases of mild oropharyngeal dysphagia, two cases of moderate to severe oropharyngeal dysphagia, and one case of severe oropharyngeal dysphagia were evidenced.
The children with microcephaly showed significant changes in swallowing and swallowing acoustics (Table 3 and Table 4). When swallowing food in liquid consistency, children with microcephaly presented incomplete verbal restraint (80%, 4/5, cases 4, 6, 15, and 19) and increased oral transit time (60%, 3/5), while when swallowing food with a pasty consistency, inadequacy in capturing the spoon was seen in 80% (4/5), with anterior labial leakage in 60% (3/5), and increased oral transit time in 60% (3/5). In addition, children with microcephaly had an average time increase of 1.11 s and an average intensity decrease of 51.58 dB. Children without microcephaly had no alterations.
Children with oropharyngeal dysphagia presented with microcephaly (p < 0.001), inadequate frequency of swallowing (0.009), and altered cervical auscultation (0.013) (Table 4).

4. Discussion

ZIKV infection in pregnancy is a concern as it is linked to catastrophic fetal abnormalities, including microcephaly, miscarriage, intrauterine growth restriction, changes in growth and development, low birth weight, growth velocity, and swallowing issues [13,14,15,16,17,18,19]. In this study, we have described the swallowing assessment of 22 children exposed intrauterine to ZIKV based on a standardized protocol and assessments and using DS. PAD-PED is a standardized protocol, developed by the Pontifical Catholic University of São Paulo, used for the clinical evaluation of OD in children, is widely used in Brazilian studies, and incorporates information provided by caregivers and clinical assessment, in addition to including an assessment of muscle tone, posture, and mobility of the stomatognathic system and a functional assessment of swallowing [39]. SD is a non-invasive, painless, low-cost method that does not expose the patient to radiation and is promising among methods for evaluating swallowing in adults, children, and babies [42,43]. SD is based on the assessment of swallowing sounds and audible cues and provides a reliable classification for screening and identifying patients with a higher risk of aspiration and laryngeal penetration [44,45]. Using these techniques, we evidenced six children with OD, across different classifications, and all of the children had microcephaly (100%).
Alterations in orofacial motricity were evidenced both in children with microcephaly and in those without microcephaly. The unanimous characteristics found in the population with microcephaly during the motricity evaluation were parted lips, tongue mobility, and decreased cheek tone. The presence of sialorrhea and sialostasis in part of the population with microcephaly was also verified, as well as the presence of a wet voice and altered cervical auscultation during voluntary swallowing. Oliveira et al. [40] showed similar aspects when evaluating 116 children (58 children exposed to Zika virus without microcephaly and 58 children with microcephaly related to Zika virus), with microcephalic children being more likely to have an inadequate resting posture for feeding, abnormality related to movement and tonus of the stomatognathic system, and OD. In the present study, all children with microcephaly presented OD.
The functional evaluation of swallowing foods with liquid consistencies showed incomplete lip sealing and increased oral transit time, while with pasty consistencies, inadequate grasping of the spoon, increased oral transit time, increased mean swallowing time, and reduced mean intensity were seen mainly in microcephalic children. Such events may be associated with inadequate neuromuscular skills and neurological damage of cortical origin in children with microcephaly [46,47]. A previous study carried out with children exposed to ZIKV showed that four microcephalic children (two of which are part of this case description, case 4 and 19, Supplementary Table S1) presented important neurological changes that were reflected in delays in neuropsychomotor development (delays in cognitive, language, motor, and psychosocial abilities), spastic tetraparesis, changes in imaging examination (deficits in social interaction, deficits in muscle strength, muscle tone abnormalities, hyperreflexia, osteotendinous, cranial nerve abnormalities, and epilepsy), and neuroimaging exams (with cerebral calcifications, ventricular dilatation, lissencephaly/pachygyria, cortico-subcortical atrophy, megacisterna magna, and periventricular leukomalacia) [37]. These changes in themselves are related to the inadequate transit of the food bolus from the mouth to the esophagus, due to an abnormality, generally cerebral or muscular. The involvement of the neuronal network in the cortical region and brain stem can leave the individual susceptible to OD in the oral and pharyngeal phases of swallowing [48,49].
OD has been demonstrated in individuals with spastic tetraparesis [50,51,52], mild cognitive impairment, neurological deficits, and cranial nerve abnormalities [53,54,55,56], in children with speech and language delays [57], and in diseases with reflexes and motor delay [58], muscle tone abnormalities, and deficits in muscle strength [59]. In addition, impairments of motor function and coordination of tongue movements cause a reduction in ejection pressure and the impairment of effective swallowing, leading to an accumulation of food in the oral and pharyngeal cavity, responsible for cervical sound changes during and after swallowing [60].
One child (case 7), in this series of cases, had a normal head circumference at birth and microcephaly during evaluation and other follow-up visits. This child had neurological and swallowing functional inadequacy. This child was exposed in utero; however, we did not evaluate factors (including genetics, perinatal injury, and postnatal injury) that could also have justified postnatal microcephaly. In general, the prognosis is worse for children who have had an intrauterine infection or have a chromosomal or metabolic abnormality [61].
OD induced by ZIKV affects growth and psychomotor development, leading to important deleterious effects on child development, especially related to growth and weight [62]. In the present study, we did not evaluate the children’s weight during the speech–language pathology assessment. However, one cohort, which included much of the sample described here (Supplementary Table S2), was described to show growth velocity (GV) and nutritional status based on World Health Organization standards of children exposed to ZIKV during pregnancy [17]. A similar frequency of low GV was shown across microcephalic and non-microcephalic children. Furthermore, the authors showed that children with changes in GV showed changes in neurological exams, although these were not statistically significant, when compared to children with adequate GV. Neurological changes were related to OD.
In this study, it was not possible to perform acoustic analyses of swallowing foods of all consistencies, due to acceptance of the food, non-introduced consistencies, and the user using an alternative feeding route. The average intensity in the liquid, pasty, and solid consistency was below expectations, demonstrating the decrease in muscle strength during the swallowing process; furthermore, in foods with a pasty consistency, the oral transit time was increased with a greater impact on children with microcephaly, correlating with the findings of clinical speech therapy assessment.
This study has limitations that are inherent of case reports. For example, in this series of cases, we only evidenced disorders in the oral and pharyngeal phases of swallowing due to the use of a non-invasive method. The use of invasive methods, such as videofluoroscopy and fiberoptic endoscopic swallowing, are more effective for exploring the dynamics, changes, safety, and efficacy of swallowing, as well as selecting and evaluating specific therapeutic strategies [63]. However, through the pediatric dysphagia clinical evaluation protocol 2014 and acoustic analysis with DS, two simple methodologies, we highlighted OD and its degrees of involvement. Due to the ease of implementation, these two methodologies can guide the first Rehabilitation for Swallowing Disorder procedures, especially in places that lack the necessary equipment for the diagnosis of OD or are far from large health units, or when the patient is unable to travel. Another limitation is that the children were not evaluated when positive for ZIKV infection, and therefore we could not define the etiology of the ZIKV in a patient who presented postnatal microcephaly.

5. Conclusions

The findings of this study are important in showing that oral motor dysfunction can be a factor associated with reduced food intake, increased energy expenditure, risk of malnutrition, choking, broncho aspiration, and aspiration pneumonia, especially in a group of children with microcephaly. Thus, longitudinal follow-up of children exposed to ZIKV infection in the intrauterine period is necessary for providing information for the correct understanding and management of swallowing difficulties, as well as other resulting problems.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/v15122363/s1, Table S1: Neurological characteristics for microcephalic children.; Table S2: Growth velocity in children exposed to the Zika virus in the intrauterine period in Manaus, Ama-zonas, Brazil.

Author Contributions

Conceptualization, C.d.S.R. and C.B.-M.; methodology, C.d.S.R. and C.B.-M.; software, C.d.S.R. and R.S.S.; validation, C.d.S.R. and C.B.-M.; formal analysis, T.D.d.A., D.C.B.-d.-S., C.d.S.R. and C.B.-M.; investigation, T.D.d.A., C.d.S.R., R.K.S.S. and C.V.-R.N.; resources, C.d.S.R. and C.B.-M.; data curation, C.d.S.R.; writing—original draft preparation, C.d.S.R., C.V.-R.N., E.d.A.A., L.H.G.M. and C.B.-M.; writing—review and editing, C.d.S.R., R.K.S.S., C.V.-R.N., R.H.O., D.d.M.B., A.K.N.d.O.M., K.P.d.O.F., E.d.A.A., L.H.G.M., L.d.F.A.A.P.C., M.R.A.-B., D.C.B.-d.-S., S.G.B., M.d.C.C., F.E.M.-E., M.d.G.C.A., R.S.S. and C.B.-M.; visualization, C.d.S.R., R.K.S.S., C.V.-R.N., R.H.O., D.d.M.B., A.K.N.d.O.M., K.P.d.O.F., E.d.A.A., L.H.G.M., L.d.F.A.A.P.C., M.R.A.-B., D.C.B.-d.-S., S.G.B., M.d.C.C., F.E.M.-E., M.d.G.C.A., R.S.S. and C.B.-M.; supervision, R.S.S. and C.B.-M.; project management, C.d.S.R.; funding acquisition, C.d.S.R., F.E.M.-E., M.d.G.C.A. and C.B.-M. All authors have read and agreed to the published version of the manuscript.

Funding

This work was funded by Fundação de Amparo à Pesquisa do Estado do Amazonas (FAPEAM): Universal Amazonas (#002/2018); the Ministry of Health of Brazil: Programa de Pesquisa para o SUS—PPSUS (#062.01018/2018)—and Departamento de Ciência e Tecnologia—(#51/2019); and Leônidas and Maria Deane Institute (ILMD/Fiocruz Amazônia), in partnership with the Nacional Council for Scientific and Technological Development—CNPq (#400911/2018-3n). C.d.S.R. received support from the Coordination for the Improvement of Higher Education Personnel (CAPES/PROAP 1247/2022). Djane Clarys Baia-da-Silva is a national visiting fellow II of the Amazonas Research Support Foundation (FAPEAM). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Institutional Review Board Statement

The study was conducted in accordance with the Declaration of Helsinki and approved by the Research Ethics Committee of the Tropical Medicine Foundation Doutor Heitor Vieira Dourado (FMT-HVD) (protocol code: 08941019.2.0000.0005/2019).

Informed Consent Statement

Informed consent was obtained from all subjects involved in this study.

Data Availability Statement

All data are contained within the article.

Acknowledgments

We would like to thank the families who agreed to follow us on this path of acceptance, care, and construction of knowledge. We thank the Zika Project’s multidisciplinary team for working with us in monitoring the children.

Conflicts of Interest

The authors declare no conflict of interest.

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Table 1. Baseline characteristics of children exposed to the Zika virus in intrauterine and assessment by a speech therapist in Manaus, Amazonas, Brazil.
Table 1. Baseline characteristics of children exposed to the Zika virus in intrauterine and assessment by a speech therapist in Manaus, Amazonas, Brazil.
IDSexAge *Gestational Age (w)Birth Weight
(Kg)		ApgarNHSTongue TestBreathing and Heart Problems
1M35403.139AdequateChangedNo
2M39392.109AdequateAdequateNo
3F38393.609AdequateNDNo
4M37392.719AdequateNDCardiac
5M32403.059AdequateAdequateRespiratory
6M35392.929AdequateAdequateNo
7M41393.179NDNDNo
8M39392.658Not suitableAdequateNo
9F30393.159AdequateAdequateNo
10M40403.408AdequateNDNo
11M33382.749AdequateAdequateRespiratory and cardiac
12M34363.299AdequateAdequateNo
13F36403.879AdequateAdequateNo
14F33383.109AdequateAdequateNo
15F23392.758NDNDNo
16F37392.239AdequateAdequateNo
17F35392.519AdequateNDNo
18M32393.659AdequateAdequateNo
19M37382.839AdequateAdequateNo
20M2739 9AdequateNDNo
21F41392.738AdequateAdequateNo
22M41393.269AdequateNDNo
* Age at time of assessment in months, ID: identification, M: male, F: female, W: weeks, Cm: centimeters, NHS: neonatal hearing screening, and ND: not determined. Microcephalic patients are marked in gray.
Table 2. Changes in orofacial motricity and saliva through clinical evaluation speech therapy (structural and functional examination) in children exposed to the Zika virus in the intrauterine period in Manaus, Amazonas, Brazil.
Table 2. Changes in orofacial motricity and saliva through clinical evaluation speech therapy (structural and functional examination) in children exposed to the Zika virus in the intrauterine period in Manaus, Amazonas, Brazil.
LipsTongueCheekPalateVocal
Quality		Frequency of SwallowingCervical
Auscultation		OD
Classification
1Parted, tone decreased, and mobility alteredPosture and tone adequate, mobility not ratedAdequateHard inadequate and soft adequateAdequateAdequateAdequateAbsent
2Occluded, tone and mobility adequatePosture and tone adequate, mobility not ratedAdequateHard inadequate and soft adequateAdequateAdequateAdequateAbsent
3Occluded, tone adequate, and mobility alteredPosture altered, tone and mobility adequateAdequateHard suitable and soft adequateAdequateAdequateAdequateAbsent
4Parted, tone and mobility adequatePosture and tone adequate, mobility not ratedAdequateHard suitable and soft adequateAdequateAdequateAdequateMild
5Occluded, tone and mobility adequatePosture, tone, and mobility adequateAdequateHard suitable and soft adequateAdequateAdequateAdequateAbsent
6Parted, tone and mobility alteredPosture and tone altered, mobility not ratedReducedHard and soft inadequateAdequateSialorrheaAdequateModerate
7Parted, tone and mobility alteredPosture and tone altered, mobility not ratedReducedHard inadequate and soft adequateInadequateSialostasisAdequateMild
8Parted, tone and mobility adequatePosture and tone altered, mobility not ratedReducedHard and soft inadequateInadequateSialorrheaAltered (worsened after swallowing)Serious
9Occluded, tone and mobility adequatePosture, tone, and mobility adequateAdequateHard suitable and soft adequateAdequateAdequateAdequateAbsent
10Parted, tone altered, and mobility adequatePosture, tone, and mobility adequateReducedHard suitable and soft adequateAdequateAdequateAdequateAbsent
11Parted, tone and mobility adequatePosture and tone adequate, mobility not ratedAdequateHard suitable and soft adequateAdequateAdequateAdequateAbsent
12Occluded, tone and mobility adequatePosture and tone adequate, mobility not ratedAdequateHard suitable and soft adequateAdequateAdequateAdequateAbsent
13Occluded, tone and mobility adequatePosture, tone, and mobility adequateAdequateHard suitable and soft adequateAdequateAdequateAdequateAbsent
14Parted, tone and mobility alteredPosture and tone altered, mobility adequateAdequateHard inadequate and soft adequateAdequateAdequateAdequateAbsent
15Parted, tone and mobility alteredPosture and tone altered, mobility not ratedReducedHard suitable and soft inadequateInadequateSialostasisAltered (worsened after swallowing)Moderate
16Parted, tone altered, and mobility adequatePosture and tone altered, mobility not ratedAdequateHard suitable and soft adequateAdequateAdequateAdequateAbsent
17Parted, tone decreased, and mobility adequatePosture and tone altered, mobility not ratedReducedHard suitable and soft adequateInadequateAdequateAdequateAbsent
18Parted, tone and mobility adequatePosture, tone, and mobility adequateAdequateHard suitable and soft adequateAdequateAdequateAdequateAbsent
19Parted, tone and mobility adequatePosture and tone altered, mobility not ratedReducedHard suitable and soft adequateInadequatesialorrheaAltered (worsened after swallowing)Mild
20Occluded, tone and mobility adequatePosture, tone, and mobility adequateAdequateHard suitable and soft adequateAdequateAdequateAdequateAbsent
21Occluded, tone and mobility adequatePosture, tone, and mobility adequateAdequateHard suitable and soft adequateAdequateAdequateAdequateAbsent
22Occluded, tone and mobility adequatePosture, tone, and mobility adequateAdequateHard suitable and soft adequateAdequateAdequateAdequateAbsent
ID: identification. OD: oropharyngeal dysphagia. Microcephalic patients are marked in gray.
Table 3. Swallowing assessment according to food consistency in children exposed to Zika virus in the intrauterine period in Manaus, Amazonas, Brazil.
Table 3. Swallowing assessment according to food consistency in children exposed to Zika virus in the intrauterine period in Manaus, Amazonas, Brazil.
Liquid Pasty Solid
IDLip SealOral Transit TimeLaryngeal ElevationAverage TimeAverage Frequency
(Hz)		Average Loudness (dB)Lip Seal Oral Transit Time Laryngeal Elevation Average Time (s)Average Frequency (Hz)Average Loudness (dB)Lip SealOral Transit TimeLaryngeal ElevationAverage Time (s)Average Frequency (Hz)Average Loudness (dB)
1AdequateAdequatePresent1.210275.6NANANANRNANANANANANANANA
2AdequateAdequatePresent712707AdequateAdequatePresent0.5141012NANANANANANA
3AdequateAdequatePresent1.5130835AdequateAdequatePresent1.2135617AdequateAdequatePresent692528
4AdequateAdequatePresent1.2124437.8AdequateAdequatePresent1.595036.7NINININININI
5AdequateAdequatePresent9111928AdequateAdequatePresent1.17128425AdequateAdequatePresent9109732
6ChangedAdequatePresent1104488ChangedAdequatePresent1.21109782NINININININI
7ChangedIncreasedPresent1.495938.4ChangedIncreasedPresent1.4100630.4NINININININI
9AdequateAdequatePresent0.6136934.3AdequateAdequatePresent0.4102222.8AdequateAdequatePresent1.499034.4
10AdequateAdequatePresent2.4110693AdequateAdequatePresent1.586654.5AdequateAdequatePresent2.499076
11AdequateAdequatePresent1106289AdequateAdequatePresent0.7125483.2AdequateAdequatePresent0.788966.1
12AdequateAdequatePresent1122183NANANANANANAAdequateAdequatePresent1.4104076
14AdequateAdequatePresent0.43101159NANANANANANAAdequateAdequatePresent1.490361
15ChangedIncreasedPresent191472ChangedIncreasedPresent0.7891278NINININININI
16AdequateAdequatePresent0.7111979AdequateAdequatePresent1120098AdequateAdequatePresent0.7102079
17AdequateAdequatePresent0.768856NANANANANRNAAdequateAdequatePresent171939.6
18AdequateAdequatePresent0.78111069AdequateAdequatePresent1.1120156AdequateAdequatePresent1135098
19ChangedIncreasedPresent0.678067ChangedIncreasedPresent0.786030.8NINININININI
20AdequateAdequatePresent0.8112792AdequateAdequatePresent1.11123169AdequateAdequatePresent1113184
21AdequateAdequatePresent0.777454AdequateAdequatePresent0.7268569NANANANANANA
22AdequateAdequatePresent0.7577459NANANANANANANANANANANANA
Child 13 was using a nasogastric tube and child 8 was not evaluated. NA: not evaluated, NI: food supply not introduced, average frequency (Hz), average loudness (dB). Reference values: time (s): 0.8 a 1.2/average frequency (Hz) 800 to 1800/average loudness (dB): 70 a 100. Microcephalic patients are marked in gray.
Table 4. Comparison of baseline characteristics and changes in orofacial motricity and saliva and swallowing assessment in children exposed to Zika virus in the intrauterine period in Manaus, Amazonas, Brazil.
Table 4. Comparison of baseline characteristics and changes in orofacial motricity and saliva and swallowing assessment in children exposed to Zika virus in the intrauterine period in Manaus, Amazonas, Brazil.
CharacteristicOverall,
n = 22		Oropharyngeal Dysphagia Absent
n = 16		Oropharyngeal Dysphagia Present
n = 6		p
Value 1
Microcephaly5/22 (22.73%)0/16 (0.00%)6/6 (100.0%)<0.001
Sex 0.4
Male14/22 (63.64%)9/16 (56.25%)5/6 (83.33%)
Age 235 (5)35 (4)35 (6)0.6
Gestational age 0.6
361/22 (4.55%)1/16 (6.25%)0/6 (0.00%)
383/22 (13.64%)2/16 (12.50%)1/6 (16.67%)
3914/22 (63.64%)9/16 (56.25%)5/6 (83.33%)
404/22 (18.18%)4/16 (25.00%)0/6 (0.00%)
Birth weight (kg)22.99 (0.45)3.05 (0.51)2.84 (0.19)0.3
Apgar 0.3
84/22 (18.18%)2/16 (12.50%)2/6 (33.33%)
918/22 (81.82%)14/16 (87.50%)4/6 (66.67%)
Adequate NHS 19/20 (95.00%)16/16 (100.00%)3/4 (75.00%)0.2
Tongue test changed1/14 (7.14%)1/11 (9.09%)0/3 (0.00%)>0.9
Breathing and heart problems 0.6
Cardiac1/22 (4.55%)0/16 (0.00%)1/6 (16.67%)
Respiratory1/22 (4.55%)1/16 (6.25%)0/6 (0.00%)
Respiratory and cardiac1/22 (4.55%)1/16 (6.25%)0/6 (0.00%)
Inadequate vocal quality 5/22 (22.73%)1/16 (6.25%)4/6 (66.67%)0.009
Inadequate frequency of swallowing 5/22 (13.64%)0/16 (0.00%)5/6 (50.00%)<0.001
Altered cervical auscultation 3/22 (13.64%)0/16 (0.00%)3/6 (50.00%)0.013
Average time for liquids1.69 (2.22)1.90 (2.55)1.04 (0.30)0.8
Average frequency for liquids1.051 (191)1.072 (198)988 (172)0.3
Average loudness for liquids57 (27)56 (29)61 (22)0.8
Average time for pasty consistencies1.00 (0.35)0.94 (0.35)1.12 (0.36)0.3
Average frequency for pasty consistencies1.089 (209)1.151 (227)965 (91)0.075
Average loudness for pasty consistencies51 (28)51 (30)52 (26)0.8
Average time for solids2.36 (2.67)2.36 (2.67)NA
Average frequency for solids1.005 (160)1.005 (160)NA
Average loudness for solids61 (24)61 (24)NA
1 Wilcoxon rank sum exact test; Fisher’s exact test; Wilcoxon rank sum test. 2 Median (IQR) [Mean (SD)]. NA: Not avaliable
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Rodrigues, C.d.S.; Souza, R.K.S.; Rocha Neto, C.V.; Otani, R.H.; Batista, D.d.M.; Maia, A.K.N.d.O.; Filho, K.P.d.O.; Andrade, T.D.d.; Andrade Almeida, E.d.; Maciel, L.H.G.; et al. Clinical and Acoustic Alterations of Swallowing in Children Exposed to Zika Virus during Pregnancy in a Cohort in Amazonas, Brazil: A Case Series Study. Viruses 2023, 15, 2363. https://doi.org/10.3390/v15122363

AMA Style

Rodrigues CdS, Souza RKS, Rocha Neto CV, Otani RH, Batista DdM, Maia AKNdO, Filho KPdO, Andrade TDd, Andrade Almeida Ed, Maciel LHG, et al. Clinical and Acoustic Alterations of Swallowing in Children Exposed to Zika Virus during Pregnancy in a Cohort in Amazonas, Brazil: A Case Series Study. Viruses. 2023; 15(12):2363. https://doi.org/10.3390/v15122363

Chicago/Turabian Style

Rodrigues, Cristina de Souza, Raillon Keven Santos Souza, Cosmo Vieira Rocha Neto, Rodrigo Haruo Otani, Daniel de Medeiros Batista, Ana Karla Nelson de Oliveira Maia, Kleber Pinheiro de Oliveira Filho, Thais Dourado de Andrade, Emmilyn de Andrade Almeida, Luiz Henrique Gonçalves Maciel, and et al. 2023. "Clinical and Acoustic Alterations of Swallowing in Children Exposed to Zika Virus during Pregnancy in a Cohort in Amazonas, Brazil: A Case Series Study" Viruses 15, no. 12: 2363. https://doi.org/10.3390/v15122363

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