Introduction
The objectives of this study were to determine the prevalence of malocclusion among children with Zika virus-associated microcephaly (MZV) and to describe the most common malocclusion in this population.
Methods
This was a cross-sectional study including patients aged between 30 and 36 months diagnosed with MZV. Healthy children were randomly selected with the same sociodemographic characteristics as the control group. Information about arch-type, primate spaces, arch form, overbite, overjet, midline deviation, anterior crossbite, anterior open bite, and the posterior crossbite was recorded. The statistical analysis used descriptive analysis, Pearson chi-square test, and multivariate logistic regression.
Results
Forty children comprised the MZV group, and 40 comprised the control group. Our results demonstrated a significantly higher prevalence of malocclusions in children who had MZV than the control group ( P <0.001). Patients with MZV were more likely to have late eruption ( P <0.001), hypoplastic maxillary arch ( P <0.001), hypoplastic mandibular arch ( P <0.001), excessive overjet ( P <0.001), and posterior crossbite ( P = 0.004).
Conclusions
The prevalence of malocclusion was higher among children with MZV. Late eruption, hypoplastic maxillary arch, hypoplastic mandibular arch, excessive overjet, and posterior crossbite were the most common characteristics for this population.
Highlights
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Children with Zika virus-associated microcephaly (MZV) had incomplete deciduous dentition.
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Malocclusion prevalence was higher among children with MZV.
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Hypoplastic maxillary arch and hypoplastic mandibular arch were common characteristics.
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Excessive overjet and posterior crossbite were also seen in children with MZV.
The Zika virus was first identified in monkeys from the Zika Forest in Uganda in 1947; the first reported infection in humans was reported 5 years later. It was then observed that the virus was transmitted by means of a mosquito vector of the Aedes genus, mainly by the Aedes aegypti mosquito, which is also responsible for transmitting other common viruses. , , In the 1980s, mosquitoes transported the Zika virus to equatorial Asia from Pakistan to Indonesia. It continued its migration to the West, as the virus passed from Southeast Asia to the South Pacific islands, where it caused major outbreaks in 2013 and 2014. ,
The virus was identified in more than 28 countries in January 2016, affecting people bitten by the infected mosquito. Some patients have been identified after virus transmission through sexual intercourse with infected partners. It is estimated that more than 80% of those infected are asymptomatic. However, after the first reports of Zika symptoms (rash, fever, arthralgia, headache, and conjunctivitis), a subsequent increase in patients with Guillain-Barre syndrome and microcephaly was reported.
In Brazil, 1.5 million people are believed to have been infected between April 2015 and January 2016. After the emergence of the Zika virus in the country, there was a 20-fold increase in the number of neonates with microcephaly. , The states in Northeast Brazil were the most affected.
Microcephaly identified at live birth is defined as an anomaly in which the head circumference (HC) is below the standard for age and gender appropriate curves. A value of HC ≤ 32 cm measured at birth in newborns between 37 and 42 weeks of gestation is considered a sign of microcephaly. , The etiology of microcephaly may involve genetic abnormalities, syndromes, metabolic disorders, teratogens, prenatal, perinatal, and postnatal infections. However, this malformation has become much more prevalent with the recent emergence of the Zika virus. Identification of the virus in the amniotic fluid, in the newborn and placental brain, as well as in pregnant women who have shown infection symptoms strongly indicates that the viral infection affects the developing brain, resulting in microcephaly. ,
Certain congenital syndromes, disorders, and malformations may be associated with clinically significant changes in the normal growth field. Influences on occlusion development include effects on both the masticatory muscles and the skeletal morphology of the maxilla and mandible. There is consensus that changes in the deviation from the normal pattern do not have specific causes. Understanding the etiologic factors contributing to variations in dentofacial morphology is the key to developing new treatment approaches.
In terms of microcephaly associated with the Zika virus in the present study, there is no scientific evidence to describe the most common occlusal traits for this population. Therefore, the objectives of this study were to describe the prevalence of malocclusions among infants with Zika virus-associated microcephaly compared with a control group and to determine the most common malocclusion in this population.
Material and methods
This cross-sectional study was carried out at the University Hospital Onofre Lopes of the Federal University of Rio Grande do Norte in Brazil. The research protocol was sent for approval by the Research Ethics Committee of the Federal University of Rio Grande do Norte, according to the norms of Resolution CNS/MS 196/96, and was approved through opinion no. 2.574086.
The study was conducted with patients aged between 30 and 36 months diagnosed with Zika virus-associated microcephaly (MZV) infection. The infants were diagnosed at birth using the current classification, in which the HC was below the standard of curves appropriate for age and gender. The mothers’ infection with the Zika virus was confirmed by clinical symptoms or serology, all with a medical diagnosis. The study used a sample of convenience because the number of children with microcephaly whose mothers had Zika infection during pregnancy was very low. This sample size has the power to detect a significant difference of up to 28% on the basis of the “malocclusion” outcome with an estimated prevalence of 50% for healthy children in this age group. A confidence level of 95% and power (1 − β) of 85% were considered for this calculation.
The control group (non-MZV) was composed of healthy infants without any comorbidities or alterations during pregnancy. Matching sociodemographic characteristics such as sex, age, and education of the mother or responsible guardian were sought to compose the control group by reviewing medical records. Infants with MZV were taken care of at the Pediatric Outpatient Clinic of the University Hospital Onofre Lopes, whereas infants in the non-MZV group were examined in municipal nurseries in the same city.
Infants underwent an oral clinical examination after being authorized by the Free and Informed Consent Form, which was performed under artificial light by a single previously-trained examiner (B.A.A.), respecting the use of personal protective equipment and using the knee-to-knee positioning technique with the help of a comfort-seat cushion. The clinical data were measured and recorded by a trained and calibrated examiner (all kappa values for calibration were >0.8).
Number 3 clinical mirrors (Duflex Instruments, Juiz de Fora, Minas Gerais, Brazil) and a North Carolina periodontal probe (Quinelato Surgical Instruments, Rio Claro, São Paulo, Brazil) were used for the examination. The use of this probe provides high precision because it is demarcated by each millimeter, unlike other probes which have millimeter bands. All biosafety standards were strictly met.
The following occlusal/malocclusion characteristics were observed: number of clinically present teeth, arch-type, primate spaces, arch form, overbite, overjet, anterior crossbite, anterior open bite, and posterior crossbite. All data were recorded in individual clinical records.
Some variables were determined regarding their absence or presence: anterior crossbite (jaw lid/box ratio changed in the anterior region), anterior open bite (overbite ≤0), posterior crossbite (jaw lid/box ratio changed in the posterior region), primate spaces in the maxillary arch (if there were spaces between the lateral and canine incisors), and primate spaces in the mandibular arch (if there were spaces between the canines and first molars). Others such as overbite and overjet were measured in millimeters using a North Carolina periodontal probe and were later categorized. Overbite values were considered normal when between >0% and ≤65%; increased when >65% and decreased if ≤0%. Regarding the overjet, normal was considered between 1 mm and 3 mm; increased >3 mm; and decreased <1 mm. Regarding the arch-type, we followed the Baume classification (type I: the presence of interincisal diastemas; or type II: the absence of interincisal diastemas) while using the usual denominations (triangular, oval, circular or parabolic, and quadrangular) for the arch form analysis.
Medical information regarding the child’s date of birth, gestational age, sex, birth weight, and serology were collected from medical charts. Data from the mother related to Zika virus infection were also recorded. An evaluation of the sociodemographic conditions of the child and their family was conducted via a specific questionnaire completed by the parents in which some variables were included, such as the education level of the primary guardian and family income , among others. Regarding the variable family income , it was dichotomized in up to R$2000 and R$2000 and above . This cut point corresponds to 2 monthly minimum wages in Brazil in 2019, which is equivalent to $500 in the United States. In addition, questions related to nutritional habits (breastfeeding and feeding) and nonnutritional habits (pacifier and/or finger sucking) were included.
Infants with similar sociodemographic characteristics to the infants in the MZV group but born without microcephaly and whose parents authorized their participation were included in the non-MZV group. Children with an at-risk pregnancy history, low birth weight, or other systemic involvement were excluded from the nonexposed group.
Statistical analysis
A database was built using SPSS software (version 25.0; IBM, Armonk, NY) to analyze the obtained results after performing clinical exams. A descriptive analysis of all the data was initially performed to measure the absolute and percentage frequency of the categorical variables and mean and standard deviations for the quantitative variables of the exposed group. A comparison of sociodemographic characteristics was also performed between the 2 groups.
A secondary analysis consisted of comparing the occlusal characteristics between the Zika virus-exposed and nonexposed groups. We sought to evaluate the risk that microcephaly offered for each condition. The chi-square test was used to evaluate the association of the variables, and the Fisher exact test was used when it could not be applied. The prevalence ratio and its 95% confidence interval were checked as a measure of the magnitude of the association. A significance level of 5% was implemented for all tests.
A multivariate analysis using logistic regression was performed in the next step, establishing the adjustment with the variable pacifier sucking for the open bite , maxillary arch , and overjet outcomes.
Results
A total of 80 infants were included in this study, with 40 infants comprising the MZV group and 40 infants in the control group (non-MZV). The characteristics of the children with MZV are shown in Table I . Only 5 mothers did not perform the serology but had a confirmed clinical diagnosis of the disease, and therefore, entered the study. The groups did not differ in their sociodemographic data. The majority of participants in both groups were male and aged between 30 and 36 months ( Table II ).
| Characteristics | Mean ± standard deviation | Minimum/maximum |
|---|---|---|
| Duration of gestation, wk | 38.64 ± 2.21 | 30.00/42.00 |
| Birth weight of infant, kg | 2.68 ± 0.63 | 1.00/4.14 |
| HC of infant at birth, cm | 29.55 ± 2.06 | 25.00/32.00 |
| n (%) | ||
| Positive serology of the mother for the Zika virus | Yes | 35 (87.5) |
| No examination | 5 (12.5) | |
| Total | 40 (100.0) | |
| Clinical diagnosis of Zika during pregnancy | Yes | 34 (42.5) |
| No | 6 (7.5) | |
| Total | 40 (100.0) | |
| Trimester in which the symptoms manifested | First | 18 (52.9) |
| Second | 13 (16.3) | |
| Third | 3 (3.8) | |
| Total | 34 (100.0) |
| Characteristics | Microcephaly | χ 2 | P | |
|---|---|---|---|---|
| No | Yes | |||
| Sex of the infant | ||||
| Male | 22 (55.0) | 22 (55.0) | 0.000 | 1.000 |
| Female | 18 (45.0) | 18 (45.0) | ||
| Total | 40 (100.0) | 40 (100.0) | ||
| Age of the infant, mo | ||||
| 30 | 13 (32.5) | 16 (40.0) | 0.487 | 0.485 |
| 31-36 | 27 (67.5) | 24 (60.0) | ||
| Total | 40 (100.0) | 40 (100.0) | ||
| Age of the mother at the infant’s birth, y | ||||
| ≤20 | 9 (22.5) | 8 (20.0) | 0.205 | 0.977 |
| 21-25 | 10 (25.0) | 11 (27.5) | ||
| 26-30 | 8 (20.0) | 9 (22.5) | ||
| ≥31 | 13 (32.5) | 12 (30.0) | ||
| Total | 40 (100.0) | 40 (100.0) | ||
| Infant’s residence | ||||
| Parent’s house | 31 (77.5) | 37 (92.5) | 3.529 | 0.060 |
| Relative’s house | 9 (22.5) | 3 (7.5) | ||
| Total | 40 (100.0) | 40 (100.0) | ||
| Person responsible for the infant, primary guardian | ||||
| Mother | 37 (92.5) | 40 (100.0) | 3.117 | 0.077 |
| Other | 3 (7.5) | 0 (0.0) | ||
| Total | 40 (100.0) | 40 (100.0) | ||
| Education level of the primary guardian | ||||
| Illiterate or incomplete elementary education | 6 (15.0) | 6 (15.0) | 0.186 | 0.980 |
| Completed elementary education | 12 (30.0) | 11 (27.5) | ||
| Completed high school | 19 (47.5) | 19 (47.5) | ||
| Completed college or university | 3 (7.5) | 4 (10.0) | ||
| Total | 40 (100.0) | 40 (100.0) | ||
| Family income | ||||
| Up to R$2000 | 29 (76.3) | 27 (67.5) | 0.748 | 0.387 |
| R$2000 and above | 9 (23.7) | 13 (32.5) | ||
| Total | 38 (100.0) | 40 (100.0) | ||
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