Inward collapse of the nasal cavity: Perinatal consolidation of the midface and cranial base in primates

Smith, Timothy D.; Ufelle, Alexander C.; Cray, James J.; Rehorek, Susan J.; DeLeon, Valerie B.

doi:10.1002/ar.24537

Cited by 11 publications

(4 citation statements)

References 33 publications

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“…More specifically, the continuity of the median, rostral part of the sphenoid with mesethmoid cartilage is interrupted by cartilage at the sphenoethmoidal junction where the anterior cranial fossa transforms from cartilage to fibrous tissue. This type of tissue conversion is documented for other parts of the chondrocranium, such as the posterior nasal capsule (Smith, Ufelle, Cray, Rehorek, & DeLeon, in press). Our findings suggest this type of change may typify all anthropoids, although a larger series of developmental stages is needed to determine the precise mechanism of this conversion.…”

Section: Discussionmentioning

confidence: 67%

Cranial synchondroses of primates at birth

Smith

Reynolds

Mano

et al. 2020

The Anatomical Record

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Cranial synchondroses are cartilaginous joints between basicranial bones or between basicranial bones and septal cartilage, and have been implicated as having a potential active role in determining craniofacial form. However, few studies have examined them histologically. Using histological and immunohistochemical methods, we examined all basicranial joints in serial sagittal sections of newborn heads from nine genera of primates (five anthropoids, four strepsirrhines). Each synchondrosis was examined for characteristics of active growth centers, including a zonal distribution of proliferating and hypertrophic chondrocytes, as well as corresponding changes in matrix characteristics (i.e., density and organization of Type II collagen). Results reveal three midline and three bilateral synchondroses possess attributes of active growth centers in all species (sphenooccipital, intrasphenoidal, presphenoseptal). One midline synchondrosis (ethmoseptal) and one bilateral synchondrosis (alibasisphenoidal synchondrosis [ABS]) are active growth centers in some but not all newborn primates. ABS is oriented more anteriorly in monkeys compared to lemurs and bushbabies. The sphenoethmoidal synchondrosis (SES) varies at birth: in monkeys, it is a suture‐like joint (i.e., fibrous tissue between the two bones); however, in strepsirrhines, the jugum sphenoidale is ossified while the mesethmoid remains cartilaginous. No species possesses an SES that has the organization of a growth plate. Overall, our findings demonstrate that only four midline synchondroses have the potential to actively affect basicranial angularity and facial orientation during the perinatal timeframe, while the SES of anthropoids essentially transitions toward a “suture‐like” function, permitting passive growth postnatally. Loss of cartilaginous continuity at SES and reorientation of ABS distinguish monkeys from strepsirrhines.

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Section: Discussionmentioning

confidence: 67%

Cranial synchondroses of primates at birth

Smith

Reynolds

Mano

et al. 2020

The Anatomical Record

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“…The fate of the chondrocranium is complex, with much of it undergoing endochondral ossification, some parts remaining cartilaginous, some parts resorbing, and some parts undergoing breakdown of cartilaginous matrix (Maier 2000;Smith et al 2008Smith et al , 2012Smith et al , 2021bRuf 2020). By far, chondrocranial elements that ossify as elements of the basicranial region of the postnatal skull have received the greatest attention in the literature (e.g., Kodama 1986a, b).…”

Section: Discussionmentioning

confidence: 99%

“…In a broad sense, primates have an accelerated loss of anterior parts of the chondrocranium, such as the posterior nasal cupula (Smith et al 2021b). In contrast, this part of the capsule remains cartilaginous at birth in Colugo cynocephalus, Tupaia belangeri, Rousettus leschenaultia (all studied in Smith et al 2017) and in muroid rodents (Ruf 2020).…”

Section: Conclusion: Implications Of Comparative Sphenoid Ontogeny In Primatesmentioning

confidence: 99%

The chondrocranial key: Fetal and perinatal morphogenesis of the sphenoid bone in primates

Mano¹,

Wood²,

Oladipupo³

et al. 2021

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The sphenoid bone articulates with multiple basicranial, facial, and calvarial bones, and in humans its synchondroses are known to contribute to elongation of the skull base and possibly to cranial base angulation. Its early development (embryological, early fetal) has frequently been studied in a comparative context. However, the perinatal events in morphogenesis of the sphenoid have been explored in very few primates. Using a cross-sectional age sample of non-human primates (n=39; 22 platyrrhines; 17 strepsirrhines), we used microcomputed tomographic (µCT) and histological methods to track age changes in the sphenoid bone. In the midline, the sphenoid expands its dimensions at three growth centers, including the sphenooccipital, intrasphenoidal (ISS) and presphenoseptal (PSept) synchondroses. Bilaterally, the alisphenoid is enlarged via appositional bone growth that radiates outward from cartilaginous parts of the alisphenoid during midfetal stages. The alisphenoid remains connected to the basitrabecular process of the basisphenoid via the alibasisphenoidal synchondrosis (ABS). Reactivity to proliferating cell-nuclear antigen is observed in all synchondroses, indicating active growth perinatally. Between mid-fetal and birth ages in Saguinus geoffroyi, all synchondroses decrease in the breadth of proliferating columns of chondrocytes. In most primates, the ABS is greatly diminished by birth, and is likely the earliest to fuse, although at least some cartilage may remain by at least one-month of age. Unlike humans, no non-human primate in our sample exhibits perinatal fusion of ISS. A dichotomy among primates is the orientation of the ABS, which is more rostrally directed in platyrrhines. Based on fetal Saguinus geoffroyi specimens, the ABS was initially oriented within a horizontal plane, and redirects inferiorly during late fetal and perinatal stages. These changes occur in tandem with forward orientation of the orbits in platyrrhines, combined with downward growth of the midface. Thus, we postulate that active growth centers direct the orientation of the midface and orbit before birth.

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“…The bony nasal septum in adults is described to undergo endochondral ossification of the median septal part of the nasal capsule (Belden et al, 1997; Smith, Ufelle, et al, 2021). A striking thick cartilage of the nasal septum was located the near term and was sandwiched by a pair of membranous bones (the vomer and ethmoid).…”

Section: Discussionmentioning

confidence: 99%

Nasal capsule ossification: A histological study using human foetuses to find an association between the foetus and adult morphologies of the nasal wall

et al. 2023

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Recent molecular biology studies have revealed the process of nasal capsule determination. We aimed to create a fate map showing the association between the adult and embryonic components of the nasal wall and nasal capsule derivatives. We examined paraffin‐embedded histological sections between 15 mid‐term (9–16 weeks) and 12 near‐term (27–40 weeks) foetuses. Until 15 weeks, membranous ossification occurred ‘along’ the capsular cartilage, contributing to the formation of the vomer, maxilla and bony nasal septum as well as the nasal, frontal and lacrimal bones. After 15 weeks, a wide lateral part of the capsule became thin and fragmented, and degenerative cartilage was observed near the lacrimal bone, in the three conchae, and at the inferolateral end of the capsule sandwiched between the maxilla and palatine bone. The disappearing cartilages appeared to be replaced by nearby membranous bones. This type of membranous ossification did not appear to use the capsular cartilage as a ‘mould’, although the perichondrium may have a role in inducing ossification. Calcified cartilage indicated endochondral ossification in the inferior concha until 15 weeks and, later, at the bases of three conchae and around the future sphenoid sinus (i.e. the concha sphenoidalis). The capsular cartilage extended antero‐superiorly over the frontal bone and inserted into the nasal bone. At 40 weeks, the capsular cartilage remained in the cribriform plate and at the inferolateral end along the palatine bone. Consequently, less guidance from the nasal capsule seemed to provide great individual variation in the shape of the wide anterolateral wall of the nasal cavity.

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Inward collapse of the nasal cavity: Perinatal consolidation of the midface and cranial base in primates

Cited by 11 publications

References 33 publications

Cranial synchondroses of primates at birth

Cranial synchondroses of primates at birth

The chondrocranial key: Fetal and perinatal morphogenesis of the sphenoid bone in primates

Nasal capsule ossification: A histological study using human foetuses to find an association between the foetus and adult morphologies of the nasal wall

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