Identification of critical windows in early development of human upper respiratory tract and middle ear disease

Abstract

Otitis media (OM) or middle ear disease is a prevalent pediatric condition generally related to early growth of the cartilaginous Eustachian tube (CET). This study used a developmental series of dry crania to reconstruct CET and dilator tubae (DT, the muscle opening the CET) morphology. Timing and directionality of CET and upper respiratory tract (URT) growth were investigated. Traditional and 3D geometric morphometrics (GM) were used to assess bony landmarks on the crania. The series was divided using dental eruption into seven growth stages ranging from before eruption of deciduous dentition (approximately the first 6 postnatal months) to eruption of the first permanent maxillary molar (after approximately 6 years). Bony endpoints of the CET and DT were used to calculate their morphology. GM analysis showed substantial shape differences between newborns, early infants, and all later developmental stages. Univariate measures showed the largest growth change between birth and 6 months. Subsequently, CET morphology changed little in the latter half of year 1, instead maturing gradually until approximately 3 years whereas DT relative length and orientation finish growth by the end of year 1. Incongruence in slower CET growth and faster DT growth could impact CET function between 6 and 12 months and be a contributing factor of OM. Tubal aeration may improve after this time when both CET and DT morphology mature, coinciding with clinically reported drop‐off in ear infections.

Nasopharyngeal morphology contributes to understanding the “muddle in the middle” of the Pleistocene hominin fossil record

“…A clue may be found in the smaller values for this composite measure being most common among H. sapiens infants (as can be seen in the growth series) who exhibit the highest rates of otitis media as a result of their immature CET morphology and function (Bluestone, 2005; Brooks, 1969; Jerger, 1970). We extrapolated previously (Pagano et al, 2019) that the H. neanderthalensis adult condition of horizontal CET orientation may have rendered children within those populations susceptible to otitis media for longer spans of their life histories, whereas vertical CET reorientation over H. sapiens development, associated with decreasing otitis media susceptibility (Bluestone, 2005), occurs around the same time that clinically observed rates of otitis media undergo steep decline (Kaur et al, 2017; Pagano et al, 2017, 2021; Paradise et al, 1997). The larger H. neanderthalensis sample in this study corroborates previous findings (Pagano et al, 2019) as this group exhibited the infant‐like condition of more horizontal pterygoid plates relative to both the Frankfurt Horizontal Plane and the basicranium.…”

“…Morphological differences between H. neanderthalensis and H. sapiens may have also resulted in functional differences in the soft palate and CET. The extreme length of the H. neanderthalensis dilator tubae relative to the CET floor may be of special importance as the former structure is the sole dilator of the latter structure and this relationship has been shown to remain unchanged (and probably under extreme functional constraint) over H. sapiens development (Pagano et al, 2021). The consistently small ratio of CET floor length to dilator tubae length among all but one of the H. neanderthalensis would be likely to result in marked differences in CET function during life, although the exact nature of this difference remains unclear.…”

“…Adults in the growth series were used for direct morphological comparison to assess both functional and phylogenetic differences with the fossil specimens. The nonadults in the sample are also informative to functional analyses as newborns model anatomically the configuration of a vertically short, broad airway in combination with basicranial nonflexion and horizontal orientation of the choanae and CET (see Pagano et al, 2021). Any morphological similarities to newborn H. sapiens have functional implications on the upper respiratory tract (e.g., Laitman et al, 1979; Pagano et al, 2019) that may contribute to understanding of differences in character state among groups.…”

“…The degree of preservation of the medial pterygoid plates and other bony nasopharyngeal boundaries and the method by which the locations of missing or damaged landmarks were estimated have been described in some of the specimens and will not be repeated here (Pagano, 2014;Pagano et al, 2019Pagano et al, , 2021. Those not previously described are discussed in detail below.…”

“…These changes relate functionally to a reconfiguration of the upper airway that has rendered Homo sapiens the only known living species to exhibit a two-tubed aerodigestive tract in which the soft palate and epiglottis lose contact over early postnatal development (e.g., Laitman & Reidenberg, 2009;Negus, 1949). Simultaneously, growth change in these structures likely underlies the reason our species suffers uniquely and endemically from chronic otitis media and rhinosinusitis as the upper airways of infants and young children are inefficient at equilibrating middle ear pressure and clearing the middle ear cavity and paranasal sinuses (Bluestone, 2005;Bluestone et al, 2012;Pagano et al, 2017Pagano et al, , 2021.…”