Emergence of oropharyngeal, laryngeal and swallowing activity in the developing fetal upper aerodigestive tract: an ultrasound evaluation

Abstract

The developing fetal upper aerodigestive system provides the structural support for respiratory and ingestive functions necessary to sustain life at birth. This study investigated prenatal development of upper aerodigestive anatomy and the association of emerging functions as predictors of postnatal feeding skills. Biometric measures of oral, lingual, pharyngeal and laryngeal structures were obtained in fetuses 15–38 weeks gestational age using a four-plane sonographic technique. Accompanying ingestive behaviors were tallied across development. The data from 62 healthy controls were compared to seven cases at risk for postnatal feeding and swallowing dysfunction (Type II Arnold Chiari Malformation, trisomy 18, polyhydramnios, intrauterine growth restriction, Brachmann–de Lange Syndrome). Significant (p<0.001) linear regressions occurred in pharyngeal and lingual growth across gestation while ingestive behavior such as suckling emerged in a sequence of basic to complex movement patterns. Jaw and lip movements progressed from simple mouth opening to repetitive open–close movements important for postnatal suckling. Lingual movements increased in complexity from simple forward thrusting and cupping to anterior–posterior motions necessary for successful suckling at term. Laryngeal movements varied from shallow flutter-like movements along the lumen to more complex and complete adduction–abduction patterns. Fetal swallowing primarily occurred in the presence of concomitant oral–facial stimulatory activity. Significant variations (p<0.01) in the form and function of the ingestive system occurred in comparisons of gestational age-matched controls to at-risk cases. We postulate that prenatal developmental indices of emerging aerodigestive skills may guide postnatal decisions for feeding readiness and, ultimately, advance the care of the premature, medically fragile neonate.

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.