The skull is a critical factor in the development of the face and therefore the upper airway. The skull develops from a membranous and cartilaginous neurocranium (Fig. 12-1). The membranous neurocranium gives rise to the flat bones of the cranial vault, and the cartilaginous neurocranium (chondrocranium) forms the skull base. The flat bones of the neurocranium, which form sutures from edge to edge, also form fontanels where more than two bones meet. The base of the skull is formed from the cartilaginous neurocranium, which then becomes the base of the occipital bone, the sphenoid, the ethmoid and petrous bones, and portions of the temporal bone.

FIGURE 12-1 Development of the skull from neurocranium and viscerocranium contributions at 20 weeks’ gestation (lateral view). The skull base, the occipital bone, the body of the sphenoid, and the ethmoid are formed from cartilaginous neurocranium. Cell-signaling as well as geometric influences contribute to further growth of cranial and anterior facial structures.

The cranial base provides a floor for the calvarium and a roof for the face. The shaping of the skull base and contiguous structures is a dynamic process involving reciprocal influences between the cranial base, the pharynx, the face, and the primary and secondary palates. During fetal life and early childhood, neural influences predominate because of the rapid growth of the brain. During postnatal development of the airway, nasal influences play a major role, and because of speech and nutritional requirements, the pharynx also influences the development of the skull base. The anterior portion of the skull base is the roof of the nasomaxillary complex, whereas the posterior portion of the cranial base is the roof of the nasopharynx. During development, the depth of the nasopharynx increases as a result of remodeling of the palate, as well as changes in the angulation of the skull base, providing an enlarged nasal airway for the adult.

The Face

Just as the neurocranium forms the cranial vault and base, the viscerocranium forms the face and is derived mainly from cartilage of the first two branchial arches (Fig. 12-3). Ectodermally-derived neural crest cells of the developing 3- to 4-week-old embryo migrate to branchial arch mesoderm, and the face develops as a result of these massive cell migrations and their interactions. Those cells forming the frontonasal process are derived from the forebrain fold and migrate a relatively short distance as they pass into the nasal region. Those cells that form the mesenchyme of the maxillary and mandibular processes have a considerably longer distance to migrate, because they must move into the branchial arches. At 28 days postconception, the face barely shows its eventual relation to the five primordia from which it is derived: the frontonasal prominence, which is the cranial boundary of the primitive mouth (stomodeum); the paired maxillary prominences (the first branchial arch); and the paired mandibular prominences (also the first branchial arch).

FIGURE 12-3 Development of the face. Neural crest cells form around the anterior neuropore and migrate to give rise to a variety of connective and nervous tissues of the skull, face, and branchial arches. With the frontonasal prominence developing for a shorter distance than the maxillary processes, there is a longer time for clefting of the lip and palate to occur. Severe rhinencephalic malformations may be accompanied by central nervous system abnormalities as well.

The paranasal sinuses begin developing at approximately 40 weeks of gestational age. The completion of turbinate development signals the beginning of sinus development, which continues until early adult life (Fig. 12-4). Although the exact function of the paranasal sinuses is not well understood, inflammatory, infectious, and neoplastic diseases of the sinuses are of major significance to the anesthesiologist, particularly if there is functional impairment before anesthesia and surgery. Sinus disorders are often comorbidities of asthma, immunoglobulin deficiencies, cystic fibrosis, or Kartagener’s syndrome.

FIGURE 12-4 The paranasal sinuses begin their development at the end of fetal life from the mesenchyme of the lateral wall of the nasal cavity, developing into the turbinates. The completion of turbinate development signals the beginning of sinus development, which continues until early adult life.

The oral cavity—a structure without structures—where much of the anesthesiologist’s attention and skills are focused, has a complex developmental heritage. The mouth (stomodeum) appears as a slight depression in the surface ectoderm, separated from the oral cavity by the oropharyngeal membrane. This membrane ruptures at about 24 to 26 days’ gestation and the primitive foregut then communicates with the amniotic cavity. The involved germ layers are the endoderm internally and the ectoderm externally. The tongue surface arises primarily from first arch mesenchyme, with significant contributions from the third and fourth arches, hence its complex innervation by the facial nerve in the anterior two thirds and the hypoglossal nerve in the posterior one third (Fig. 12-5). The muscle bulk of the tongue arises primarily from occipital somites, explaining the hypoglossal nerve (XII) innervation and its susceptibility to injury from errant placement of dental rolls and pressure injury from overinflated LMA cuffs. The upper lip is formed by the merging of the maxillary prominences with the medial nasal prominences, with the lateral basal prominences forming the alae. The intermaxillary segment in the central portion of the upper lip area consists of a labial component (forming the philtrum), a maxillary component (associated with the four incisor teeth), and a palatal component (which becomes the primary palate).

FIGURE 12-5 The tongue is a complex structure, derived as it is from elements of the first four branchial arches. This results in the first branchial arch contributing to the anterior two thirds of the tongue (lingual nerve, a branch of the mandibular division of the fifth cranial nerve), as well as the chorda tympani from the seventh cranial nerve. The third branchial arch contributes to the posterior third of the tongue, resulting in its innervation by the ninth cranial nerve. Tongue muscles, derived from the occipital myotomes in the region of the developing hindbrain, are innervated by the twelfth cranial nerve. The foramen cecum is the pharyngeal floor diverticulum in continuity with the developing thyroid.

The palate divides the nasomaxillary complex from the oral cavity (Fig. 12-6). The palatal processes advance in a medial direction from the maxillary processes of the first branchial arch, fusing in the midline in an anterior-to-posterior sequence and uniting with the premaxilla and the developing nasal septum. The soft palate forms from continued growth of the posterior edges of these palatal processes, ending with the formation and fusion of the two halves of the uvula.

FIGURE 12-6 Formation of the primary and secondary palates, ultimately forming the floor of the nose and the roof of the mouth. The process of midline fusion occurs from posterior to anterior; clefting of the primary or secondary palate may occur in various combinations.

Clinical Correlation

Cleft lip and palate are among the most common of congenital anomalies. They may occur alone, as part of a syndrome (there are over 300 syndromes associated with facial clefting), or as a component of a sequence, (e.g., as with Pierre-Robin syndrome). Clefts of the palate may occur by the same mechanism as cleft lip or be secondary to an anatomic obstruction preventing the medial fusion of the maxillary processes. For example, the cleft palate associated with Pierre-Robin syndrome occurs when the tongue, being displaced superiorly and posteriorly as a result of mandibular hypoplasia, interferes with palatal fusion.

Closure of the cleft palate may result in insufficient tissue for development of normal length or function of the soft palate and require a posterior pharyngeal flap. Velopharyngeal insufficiency is the cause of the hypernasal speech, nasal emission, and nasal turbulence (Sidman and Muntz, 2000).

The nose originates in the cranial ectoderm, which subsequently develops into the frontonasal prominence. The superior portion of the nose is formed from the lateral nasal processes, whereas the inferior portion of the nasal cavity is incomplete until the paired maxillary processes of the first branchial arch grow anteriorly and medially to fuse with the median nasal processes. The nasal cavities extend posteriorly during development, influenced by the posteriorly directed fusion of the palatal processes, thinning out the membrane that separates them from the oral cavity. By the thirty-eighth day of development, the two-layer membrane consisting of nasal and oral epithelia ruptures and forms the choanae (posterior nares). Failure of such rupture results in choanal atresia, although these choanae are not in the same location as the definitive choanae, which will eventually be located more posteriorly. Because the normal nasomaxillary complex grows both downward and forward, however, it does explain the unexpectedly anterior location in choanal atresia given the eventual normal development of the choanae.

Clinical Correlation

Choanal stenosis is not a blockage but rather a narrowing of less than 6 mm. Choanal atresia is also associated with various syndromes in up to 70% of patients, of which colobomas, heart disease, atresia of the choanae, retarded growth, genital anomalies, ear anomalies (the CHARGE association) is the major one. Repair of this form of choanal atresia may be more complicated, requiring a tracheostomy in infancy as an initial stage and more definitive repair later.

Bilateral choanal atresia is apparent immediately in the neonatal period because infants are obligate nasal breathers. These infants have respiratory distress, paradoxical cyanosis (crying relieves the cyanosis), and failure to thrive. The natural position of the tongue promotes obstruction that is relieved by an oral airway or a McGovern nipple (a standard nipple with an enlarged hole). Unilateral atresia often appears later (2 to 5 years of age) with rhinorrhea and chronic mucoid discharge and is often misdiagnosed. Because the intraoral airway is foreshortened as a result of the abnormally anterior choanal aperture, upper airway obstruction while breathing is common, and visualization of the laryngeal structures may be more difficult. Long-standing choanal atresia may also lead to obstructive sleep apnea.

The face, specifically the maxilla and mandible, grows in a dynamic fashion throughout childhood under the influence of bony deposition and resorption, soft-tissue contouring, and hormonal influences. In a reciprocal fashion, the skull base or neurocranium influences midfacial development via the growth of the sinuses, which in turn influence the skull base. Displacement of these structures of the nasomaxillary complex occurs in horizontal, vertical, and anteroposterior axes. These changes ultimately affect the proportions of the face and the morphology of all of the facial structures, including the upper airway.

The Branchial Apparatus

Branchial Arches

The branchial apparatus consists of four branchial arches visible on the surface of the embryo, as well as fifth and sixth arches that cannot be seen on the surface. Branchial pouches and clefts are likewise numbered craniocaudally (Fig. 12-7). The first branchial arch (Meckel’s) cartilage is the position of the future mandible, as well as the eventual malleus and incus. The second branchial arch cartilage produces the stapes, the styloid process, the stylohyoid ligament, and the superior portion of the body of the hyoid. The other branchial arch cartilages contribute to the inferior portion of the hyoid as well as the thyroid cartilage.

FIGURE 12-7 The branchial arches, pouches, and clefts. The musculature of each arch is supplied by the (cranial) nerve of its origin; the first arch by the mandibular division of the fifth cranial nerve, as well as the chorda tympani division of the seventh cranial nerve. The seventh cranial nerve supplies the second arch, the ninth cranial nerve the third arch, and the tenth and eleventh cranial nerves the remaining arches. Branchial clefts, when they fail to obliterate during normal development, may result in sinuses or cysts that communicate with the oropharynx through various pathways in the neck.

Striated muscles are also formed in the respective branchial arch mesenchyme. Myoblasts differentiate and migrate to various parts of the head and neck, where they form the muscles of mastication and facial expression, each retaining their original nerve supply. Although muscular actions in the head and neck are thought of as far removed from the origin and course of the cranial nerves, fetal nerves that supply the branchial arch derivatives only have a short distance to travel from the brain. The trigeminal (V) nerve supplies the skin covering the parts of the face derived from the first branchial arch maxillary and mandibular divisions (the ophthalmic division does not make a contribution). The facial (VII) nerve supplies the muscles derived from the first arch. The nerve of the third branchial arch is the glossopharyngeal (IX) nerve. Two branches of the vagus (X) nerve supply the remaining branchial arches. The superior laryngeal nerve innervates derivatives of the sixth branchial arch.

Branchial Pouches

The first branchial pouch develops into the tubotympanic recess, becoming the auditory tube and the middle ear cavity (Fig. 12-8). The cavity of the second branchial pouch is largely obliterated as the palatine tonsil develops, but part of it remains as the tonsillar fossa. The endoderm of the second branchial pouch becomes the surface epithelium of the tonsil and the lining of its crypts, with the mesenchyme around the pouch differentiating into lymphoid tissue. The endoderm of the dorsal part of the third branchial pouches differentiates into the inferior parathyroids, and the ventral parts unite to become the thymus. The paired parathyroid glands develop from separate pouches, with one pair derived from the third and the other from the fourth branchial pouch. At the seventh week of development, the parathyroid glands migrate caudally from their respective branchial pouches, with the third pouch parathyroids moving more caudally than the parathyroids of the fourth pouch. Accessory parathyroid tissue may be left along the line of migration. The endoderm of the fourth branchial pouches differentiates into the superior parathyroid glands, and the ventral parts develop into the ultimobranchial bodies, the calcitonin-secreting portion of the thyroid.

FIGURE 12-8 The tympanic cavity develops from the tubotympanic recess, an outgrowth of the first pharyngeal pouch, which extends laterally, contiguous with the external auditory canal having formed from the first pharyngeal cleft.

Branchial Clefts

Between the first and second arches, the first branchial cleft forms the external ear, which is the only normal structure to arise from a branchial cleft. However, if the second arch does not grow caudally over the third and fourth arches, as it normally should, then the second, third, and fourth clefts can remain as branchial fistulas, in contact with the skin surface between the clavicle and the mandible. Incomplete or arrested development of the branchial clefts may result in residual cysts, sinuses, and fistulas that may eventually become infected and require excision. The clinical significance of the specific embryology is that characteristic locations are of important surgical significance.

Clinical Correlation

The second branchial arch may occasionally fail to bury the second, third, and fourth branchial clefts completely, resulting in a cervical sinus communicating with the surface of the skin, and forming a branchial sinus, which may also contain a branchial cyst. These sinuses may be accompanied by a draining infection along the anterior border of the sternocleidomastoid muscle, requiring complete surgical dissection and removal. It is easy to understand embryologically how these tracts can open into the pharynx just posterior to the tonsils and may even pass between the external and internal carotid arteries.

The thyroid begins as a thickening of the endoderm of the floor of the pharynx, in the midline between the first and second pouches, at the foramen cecum. A thin connection, the thyroglossal duct, remains attached to the oral cavity, and its point of attachment marks the origin of the thyroid gland. The thyroid descends along the thyroglossal duct and reaches the level of the first tracheal ring at about the seventh week of gestation (Fig. 12-9). The thyroglossal duct is then normally obliterated. Accessory thyroid tissue may be deposited anywhere along this path; on the other hand, failure of the thyroid to descend may result in a lingual thyroid.

FIGURE 12-9 Descent of the thyroid along the thyroglossal duct. A lingual thyroid is the most common form of incomplete descent and is found inferior to the foramen cecum, where it may interfere with swallowing as well as breathing, particularly during anesthetic induction in infants.

Anomalies associated with abnormal development of the branchial arches are varied, with a range of complexity and airway implications. Whereas too much variation among anomalies exists, an appreciation of the developmental anatomy explains (and helps the anesthesiologist anticipate) the following situations:

1. Unilateral or bilateral hypoplasia of upper airway structures, which may result in a small and hypomobile mandible, choanal stenosis or atresia, and hypoplastic or nonexistent sinuses.

2. Fusions or other abnormalities of various cervical vertebrae.

3. Cleft palate may be the result of failure to fuse, or it may be associated with hypoplastic mandibles and glossoptosis (Pierre-Robin syndrome) or hemifacial microsomia (Goldenhar’s syndrome).

4. Obstructive sleep apnea, which may result from chronic upper airway obstruction as a result of decreased available cross-sectional diameter of the airway with a relatively large volume occupied by the tongue and pharyngeal musculature, as well as an abnormally positioned palate.

The Larynx

Development of the larynx begins at approximately 3 weeks of gestational age with the formation of the laryngotracheal tube from the ventral wall of the foregut. The laryngotracheal tube then grows caudally into the splanchnic mesoderm on the ventral surface of the foregut, dividing into the right and left lung buds. The epiglottis begins to form from the hypobranchial eminence of the third and fourth arches at approximately 30 to 32 days’ gestation. The aryepiglottic folds develop from the lateral boundaries of the fourth arch along a line from the hypobranchial eminence (epiglottis) to the arytenoid eminence of the sixth arch. Incomplete development at this stage may produce varying degrees of persistent laryngeal cleft (Fig. 12-10). A definite larynx may be seen by 41 days’ gestation. (Fig. 12-11).

FIGURE 12-10 Laryngeal cleft, in various grades, results from a persistent communication between the trachea and esophagus, most commonly at the cranial end. Type I lesions are localized to the interarytenoid space superior to the vocal cords; type II lesions involve a partial cricoid cleft. Types III and IV lesions traverse the cricoid completely.

FIGURE 12-11 Development of the larynx. The epiglottis begins to form from elements of the third and fourth branchial arches at approximately 30 to 32 days of gestation, and early arytenoids cartilages can be identified on both sides of the laryngeal slit at this time as well. Incomplete development at this early stage may produce variable degrees of laryngeal cleft.

The cricoid and thyroid cartilages begin to develop before the arytenoid cartilages, with chondrification starting at about 7 weeks of gestation. As the thyroid cartilage develops, the glottis deepens, and the true vocal cords align within the thyroid laminae. Failure of the true vocal cords to split to form the primitive glottis at 10 weeks of gestation results in congenital atresia of the larynx or more often, a complete or partial congenital laryngeal web. Although webs may be supraglottic or subglottic, most occur at the level of the glottis. Congenital cysts of the supraglottic region are possibly remnants of the third branchial pouch and lie superior to the derivatives of the fourth arch. By the tenth to eleventh weeks of gestation, the major structures of the larynx have developed and the cartilages are chondrifying. If the separation of the esophagus and trachea is slightly delayed and the margins of the laryngotracheal groove fail to fuse adequately, the rapidly growing trachea separates the proximal and distal esophagus, resulting in the most common form of proximal esophageal atresia and distal tracheoesophageal fistula.

Eckenhoff’s (1951) review of the anatomy of the pediatric larynx has influenced more than a generation of pediatric anesthesiologists with regard to the selection of endotracheal tube size based on the concept of the narrowest (fixed) portion of the upper airway being the level of the cricoid cartilage, or the “funnel-morphing-into-cylinder” concept. Litman et al. (2003) examined laryngeal shape in sedated children undergoing MRI and determined that under sedated conditions with tonic maintenance of laryngeal shape, it is more cylindric than funnel-shaped, as it is in adults, and that the narrowest portion of the airway is at the level of the vocal cords. Furthermore, they concluded that there is no change in this relationship from childhood to adulthood. This finding has been confirmed by video-bronchoscopic imaging in anesthetized and paralyzed children as well and provides an intriguing challenge to traditional teaching (see Chapter 3, Respiratory Physiology) (Dalal et al., 2008, 2009). The adjudication of these disparate concepts, as well as the confirmation in both reports that the cricoid opening is elliptic rather than circular in shape, with the narrowest transverse diameter, help support the transition over the last 10 to 15 years to the common use of cuffed endotracheal tubes with a smaller diameter rather than tightly (or “appropriately”) fitted, uncuffed endotracheal tubes. Moreover, advances in materials and design have allowed the development of thin-walled tubes with shorter, polyurethane cuffs, which provide an equivalent seal at a lower mucosal pressure (Dullenkopf et al., 2005). At this point, the increasingly routine use of cuffed endotracheal tubes, with appropriate care, appears to result in fewer repeated laryngoscopies and reintubations, less postintubation croup and less contamination in the operating room, and lower total fresh-gas flows.

Developmental physiology

The Upper Airway

It is almost axiomatic in pediatric training to be told that the infant is an obligate nasal breather, and the reasons are best understood by developmental anatomy. The epiglottis is located in a more cephalad position relative to the other mobile soft-tissue components of the oral cavity, the tongue and soft palate, and their close approximation even during normal respiration may impair transoral breathing. Nasal resistance may provide up to 50% of total airway resistance and varies depending on alar orientation, the pyriform aperture, the nasal cavity, and the choanae. This is of practical importance to the pediatric anesthesiologist particularly when anatomic or even therapeutic (e.g., nasogastric tube) obstructions are present, because airway resistance is significantly increased and therefore respiration may be compromised.

The tongue, palate, pharynx, epiglottis, and larynx all have to work together to accomplish feeding and breathing. With postnatal growth, the mandible enlarges, descends, and protrudes, and the oral cavity enlarges vertically. The tongue occupies a more anterior position as the oral cavity and pharynx grow, and the larynx descends from its C2 position in the neck to C4 after one year of age. The clinical usefulness of the high-lying larynx is that it places the epiglottis into contact with the soft palate, allowing the infant to be a nasal breather while sucking and swallowing. With the growth of the oral cavity and the rearrangement of intraoral architecture during the first few months of life, infants convert from obligate nasal breathing to nasal and oral breathing.

Isono (2006) has reviewed the physiology of airway maintenance at the pharyngeal level and described the pharynx as a collapsible air-filled tube surrounded by soft tissues enclosed in a rigid box of bony structures, the mandible and vertebrae, with the lumen of the tube determined by the balance of the soft-tissue mass and the size of the surrounding rigid box. This simple approach explains the success of routine clinical airway maneuvers—continuous positive airway pressure (CPAP) serving as a pneumatic stent for the collapsed air-filled tube and surrounding soft tissue, and anterior displacement of the jaw serving to enlarge the rigid box. An oral airway displaces the base of the tongue anteriorly, thereby increasing the transpharyngeal luminal space and moving the base of the tongue away from the prevertebral bodies. Anesthetics, of course, depress the integrity of pharyngeal muscle tone through a variety of mechanisms, including the attenuation of neural input caused by the loss of consciousness and the decrease in tone of the diaphragm and intercostal musculature. The tongue and its muscular attachments such as the genioglossus, geniohyoid, sternohyoid, sternothyroid, and thyrohyoid are affected as well. All of this conspires to narrow the pharyngeal airway, more so in infants and small children than adults, especially during the first year of life (Isono et al., 2000). Adults are more equipped than children to defend against these effects, because they possess a more competent negative pressure reflex serving to augment pharyngeal tone, although the negative pressure reflex has been shown in infants younger than 1 year old as well (Thach et al., 1989; Horner et al., 1991). In addition, the progressive increase in pharyngeal cross-sectional area during the first year of life is positively influenced by the growth of the mandible and maxilla.

Pharyngeal airway obstruction has long been recognized as a significant component of the clinical entity called laryngospasm, and the application of CPAP, whether applied transnasally or transorally, depresses pharyngeal muscle tension and provides a mechanical pneumatic stent for the upper airway (Fink, 1956; Alex et al., 1987). This is a subtle component of the routine technique used by experienced pediatric anesthesiologists in applying gentle amounts of positive pressure during the induction phase, especially with infants and small children.

The fetus is an experienced swallower, well practiced from the age of 10 to 11 weeks’ gestation, with suckling following at 18 to 24 weeks’ gestation. This is fortunate, because coordination of this highly complex task is dependent on practice in utero and learning in pre- and postnatal life. However, breathing, even in utero, is a relatively late event, occurring at about 32 to 37 weeks’ gestational age, and premature infants show their lack of experience with significant discoordination between swallowing and breathing, as do children who are neurologically impaired (Goldson, 1987; Arvedson et al., 1994).

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