Emergence of oropharyngeal, laryngeal and swallowing activity in the developing fetal upper aerodigestive tract: an ultrasound evaluation
Introduction
At birth, the normal-term neonate is able to suck and swallow in a manner sufficient for life-sustaining nutritional intake. The integrity of these postnatal skills, however, is dependent on the prenatal development of orofacial, pharyngeal and laryngeal anatomy [1], [2], [3], [4]. Together, these developing upper aerodigestive structures support the emergence of respiratory and gastrointestinal tract functions that serve the neonate as well as the fetus. For example, fetal swallowing contributes to homeostatic regulation of amniotic fluid volume, the acquisition and recirculation of intrauterine solutes and overall fetal growth [5], [6], [7], [8], [9]. These responses are influenced by a variety of maternal–fetal conditions (e.g., amniotic fluid levels, fetal hypotension, plasma osmolarity changes, maternal hypoxemia) that may alter intrauterine aerodigestive functions and potentially affect the development of behaviors necessary for extrauterine feeding, swallowing and respiration [8], [10], [11], [12]. Congenital anomalies such as tracheoesophageal fistula, cleft palate or laryngeal stenosis are known to disrupt sucking and swallowing abnormalities at birth [13]. Further, postnatal feeding and respiratory dysfunctions are associated with complications from premature birth and low birth weight [13], [14]. The postnatal implications of these prenatal conditions suggest that the evaluation of fetal aerodigestive structures and observation of emerging ingestive behaviors may be useful as markers of fetal health and predictors of potential neonatal compromise [15], [16]. However, how this system develops and when its integrated functions emerge has not been fully studied in the living human. Furthermore, specific intrauterine conditions that may lead to postnatal ingestive deficits have not been examined across gestation.
With the introduction of real-time ultrasound imaging, a noninvasive method is now available to examine these conditions in the living human fetus. A series of sonographic studies have already documented the growth of specific orofacial, pharyngeal and lingual structures [17], [18], [19], [20]. Correlations between growth and gestational age have been reported using measures of cheek-to-cheek diameter [21], mandibular size [22], [23] and lingual dimension [24], [25]. Parameters of normal [26] and abnormal [27] swallowing function in relation to specific structural abnormalities such as micrognathia [28], cleft palate [29] and esophageal atresia have been documented [30]. These studies have provided important information on the emergence of swallowing-related behaviors in specific fetal populations. However, the association between the growth of such structures and the development of their ingestive functions has not been fully evaluated. Few comparisons of developing upper aerodigestive form and function exist between the healthy and the compromised (or ‘at-risk’) fetus.
Thus, the purposes of this study were to investigate prenatal development of the upper aerodigestive tract and to examine the differences in emerging functions between healthy and “at-risk” fetuses. We postulated that prenatal developmental indices of emerging aerodigestive skills might provide data to guide postnatal decisions for feeding readiness and, ultimately, advance the care of the premature, at-risk infant. Specific oral, lingual, pharyngeal and laryngeal structures were measured in fetuses 15–38 weeks gestational age (GA). We used a new sonographic imaging method to document prenatal development of the aerodigestive system and evaluated whether the enhanced resolution of this imaging technique provided earlier detection of fetal anomalies and greater accuracy in measures of anatomic growth. We hypothesized that the ‘at-risk’ fetus would demonstrate reductions in both the form and function of the ingestive system.
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Subjects
Mothers (mean age 32.2 years, age range 19–42 years) with singleton pregnancies were selected by the attending maternal –fetal specialist physician at the National Naval Medical Center Prenatal Assessment Center. All volunteers participated based on informed consent procedures approved by the National Naval Medical Center at Bethesda (NNMC) and the National Institutes of Health (NIH). The maternal/fetal diagnosis and the clinical sonographic findings were used to categorize the mother/fetus in
Results
Data are presented from 69 cases (62 normal controls, 7 at-risk test cases). The mean gestational age of all fetuses based on last menstrual period as confirmed by sonographic measures was 24 weeks 3 days gestational age (GA, range 15w1d–38w3d). Of the 69 cases, 65 were term births, 3 were premature (one control, two at-risk cases) and 1 at-risk case resulted in miscarriage. Trends related to fetal activity and the time of the exam were not found. Follow-up parental interviews and chart reviews
Discussion
This study examined the emergence of upper aerodigestive behaviors concomitant with the growth and development of orofacial, lingual, pharyngeal and laryngeal structures. Upper aerodigestive anatomy and related ingestive behaviors were observed in our youngest subjects (15 weeks GA) using the four-part ultrasound evaluation supplemented by power Doppler sonography. In the 62 fetuses studied, statistically significant increases in pharyngeal and lingual growth occurred across gestation. Despite
Acknowledgements
This work is part of an on-going study at NNMC (Protocol #B99-089) and NIH/NICHD (Protocol 00-CC-081). The authors would like to thank the many parents who have participated with their children in this project.
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