Abstract
There seems to be no information on when and how the nasal capsule cartilage is divided into the lateral nasal cartilage (LNC) and greater alar cartilage (GAC). Likewise, there is no information of timing and sequence of development of the medial crus of GAC. We examined histological sections from 22 human fetuses with 45–350 mm of crown-rump length (approximately 9–40 weeks of gestational age). The LNC and GAC were separated from the antero-inferior marginal part of the nasal capsule cartilage at 10–12 weeks. The initial sesamoid was a wavy bar and it did not accompany a joint cavity. The LNC did not make an end-to-end attachment to the septal cartilage and these cartilages were separated by sesamoid cartilages in levels below the nasal bone. However, we did not find a sesamoid between the LNC and GAC. After 27 weeks, the medial crus of the GAC was seen in the antero-inferior side of the septal cartilage. Thus, independently from the septal cartilage, it seemed to develop secondarily from the GAC main part. Relative to the nasal bone, the LNC at late-term was small in the supero-inferior axis. The vomeronasal cartilage was distant from and located in the posterior side of the external nasal cartilages and vestibulum. At birth, the LNC as well as the GAC including its medial crus seemed to be still separated from the septal cartilage. Their connections most likely establish postnatally with tight interdigitation of highly flexed cartilage ends. No lesser alar cartilage appeared at late-term.
Keywords: Lateral nasal cartilage, Alar cartilages, Nasal septum, Vomeronasal organ, Human fetus
Introduction
According to Drumheller [1], cartilages of the external nose are all derived from a single initial cartilaginous framework (=nasal capsule cartilage and septal cartilage) that is divided and partly absorbed to form the lateral nasal cartilage (LNC), the greater alar cartilage (GAC) and lesser alar cartilage (LAC) and a pair of sesamoid cartilages. Indeed, using sagittal sections, Yamamoto et al. [2] demonstrated the LNC and GAC as an antero-inferior “continuation” of the septal cartilage. However, because the external nasal cartilages are highly curled medially or internally, sagittal sections likely provide a limited information. In adults, previous studies demonstrated the absence of a simple continuation between the septal and alar cartilages [1, 3].
Fig. 1 and Table 1 show our six questions (Q1–Q6) in the fetal development and growth of the nasal cartilages. Since it likely grows along the LNC, a fetal nasal bone might cover the smaller proportion of the LNC relative to the adult’s morphology (Q1). The LNC is not connected to the septal cartilage in adults. However, because both are derived from the nasal capsule cartilage, the LNC might make an articulation with septal cartilage in fetuses (Q2). Sesamoid cartilages are well known in the extremities and they accompany a joint cavity for the functional role as a tendon-bone interface (e.g., a foot sesamoid reported by Jin et al. [4]). Likewise, the nasal sesamoid cartilage might have a functional role for an articulation between the LNC and GAC (Q3). The bilateral GACs sandwich the septal cartilage in adults, but there is no information in fetuses (Q4). The GAC is composed of a lateral main part (=lateral crus) and a highly curved medial part (=medial crus) [1, 5-7]. Because of the median position attaching to the septal cartilage [3], the medial crus might develop independently from the main part of the GAC (Q5).
Fig. 1.
Topographical anatomy of the external nasal cartilages and nearby bony structures in adults. Lateral view of the nose. The external nasal cartilages are superimposed into the median structures including the nasal septum cartilage (NS), the vomer (VO), the maxilla (MX) and the incisive bone. The nasal bone (NB) covers the lateral nasal cartilage (LNC). The greater alar cartilage (GAC) has a medially-curved part surrounding the vestibulum of nose. The sesamoid cartilages (SCs) may be considered to exist between the LNC and GAC. The present introduction postulates six concrete questions (Q1–Q6; Table 1). LAC, lesser alar cartilage.
Table 1.
Questions at the beginning of this study
| Order | Question contents |
|---|---|
| Q1 | Does the nasal bone develop and slide along the LNC? |
| Q2 | Does the LNC articulate with the septal cartilage? |
| Q3 | Does the sesamoid cartilage have a functional role between the LNC and GAC? |
| Q4 | Does the septal cartilage reach the GAC and sandwich the latter at the antero-inferior end? |
| Q5 | Does the “medial crus” of the GAC develop independently from the main part? |
| Q6 | Are the median parts of the alar cartilages near or distant from the vomeronasal cartilages? |
GAC, greater alar cartilage; LNC, lateral nasal cartilage.
Finally, previous researches of the external nasal cartilages did not address the topographical relationship with the vomeronasal cartilages (=Jacobson’s cartilages). The latter was considered to exist near or adjacent to the vomeronasal organ in human fetuses [8, 9]. However, there might be no photographic demonstration showing topographical relation of these cartilages (Q6). Consequently, to resolve these questions, the aim of this study was to examine the fetal development and growth of the external nasal cartilages using both sagittal and horizontal sections.
Materials and Methods
This study was conducted in accordance with the Declaration of Helsinki 1995 (as revised in 2013). We examined paraffin-embedded histological sections from 10 midterm fetuses (45–125 mm crown-rump length [CRL]; approximately 9–16 weeks of gestational age [GA]) and 12 late-term fetuses (216–350 mm CRL; approximately 27–40 weeks of GA). The serial histological sections of the 10 midterm fetuses were part of the large collection kept at the Department of Anatomy of the Universidad Complutense, Madrid, and were the results of miscarriages and ectopic pregnancies from the Department of Obstetrics of the University. The family had donated the fetus to the university. They had been prepared serially and stained with hematoxylin and eosin (H&E) or azan. The sectional planes were sagittal (4 specimens) or horizontal (6 specimens). This study was approved by the Ethics Committee of Complutense University (B08/374).
The 12 late-term fetuses were part of the collection of the Department of Anatomy, Akita University and had been donated by their families to the Department in 1975–1985 and preserved in 10% v/v neutral formalin solution for more than 30 years. Data on these specimens included the date of donation and the number of gestational weeks, but did not include the name of the family, obstetrician or hospital or the reason for abortion. The use of these specimens for research was approved by the Akita University Ethics Committee (No. 1428) and the fifth author (G.M.) was one of members of the registration. Before routine procedures for embedding in paraffin, the fetal head specimens were decalcified by incubation at room temperature in Plank-Rychlo solution (AlCl2/6H2O, 7.0 w/v%; HCl, 3.6 v/v%; HCOOH, 4.6 v/v%) for 3–7 days. Sagittal sections (5 specimens) and horizontal sections (7 specimens) of the head were prepared at 0.1–0.2 mm interval with 7–10 micron in thickness, and stained with H&E. The horizontal sections covered levels from the lower part of the nasal bone to the upper lip muscles. All photographs were taken with a Nikon Eclipse 80 (Nikon). These sections of the late-term fetuses had been prepared for our recent study of the orbital contents and sphenoid [2, 10, 11].
Results
Observations of horizontal sections
A cage-like nasal capsule cartilage was seen in midterm fetuses (specimens smaller than 125 mm CRL or earlier than 16 weeks of GA; Figs. 2, 3). At the stages, the cage-like cartilage (future LNC and GAC) was connected to the septal cartilage in the superior plane (Figs. 2A, E, 3A, E). Inferiorly, sesamoid cartilages appeared and interposed between the septal cartilage and a lateral cartilaginous wall (Figs. 2B, F, 3B, H). More inferiorly, the anteriorly-located GAC and the posteriorly-located LNC were divided (Figs. 2C, G, 4D). The GAC corresponded to the antero-inferior end of a cage of the nasal capsule cartilage. Therefore, inferiorly, the sesamoid was located between the septal cartilage and GAC (Figs. 3I, 4B).
Fig. 2.
Lateral nasal, greater alar and sesamoid cartilages (SCs) become separated from a cage of the nasal capsule cartilage. H&E staining (A–C, F) and azan staining (D, E, G, H). Horizontal sections. Panels (A–D), a fetus with 72 mm crown-rump length (CRL); panels (E–H), a fetus with 82 mm CRL. Panels (A) and (E) (or D, H) display the most superior (or inferior) plane in each of the specimens. The upper side of each panel corresponds to the anterior side of the head. A cage-like nasal capsule cartilage (NC) is connected to the nasal septum cartilage (NS) in the superior plane (A, E). Inferiorly, SCs (B, F) appear between the septal cartilage and a lateral cartilaginous wall. More inferiorly, the greater alar cartilage (GAC) is separated from the lateral nasal cartilage (LNC; C, G). Panels (A, C–E, G, H) or (B, F) were prepared at the same magnification. (A, B) Scale bars=1 mm. IC, inferior concha; MX, maxilla; NLD, nasolacrimal duct; VES, vestibulum of the nose; VNC, vomeronasal cartilage; VNO, vomeronasal organ; VO, vomer.
Fig. 3.
Greater alar cartilage corresponding to the inferior end of a cage of the nasal capsule cartilage. H&E staining. Horizontal sections. A fetus with 105 mm crown-rump length. Panel (A) (or F) displays the most superior (or inferior) plane in the figure. The upper side of each panel corresponds to the anterior side of the head. Squares in panels (A–C) are shown at the higher magnification in panels (G–I), respectively. A cage-like nasal capsule cartilage (NC) is connected to the nasal septum cartilage (NS) in the superior plane (A). Inferiorly, the greater alar cartilage (GAC; D–F) is separated from the other cartilages. A pair of wavy sesamoid cartilages (SCs; H, I) interposes between the GAC and NS. Panels (A–C), (D–F), and (G–I) were prepared at the same magnification. (A, D) Scale bars=1 mm. (H) Scale bar=0.1 mm. VNO, vomeronasal organ; LNC, lateral nasal cartilage; VES, vestibulum of the nose; VNC, vomeronasal cartilage.
Fig. 4.
Delayed development of the medial crus in the antero-inferior side of the greater alar cartilage (GAC). H&E staining. Horizontal sections. A fetus with 230 mm crown-rump length (same specimens as shown in Fig. 5). Panel (A) (or H) displays the most superior (or inferior) plane in the figure. In (A), 0.5 mm inferior to Fig. 5C, the lateral nasal cartilage (LNC) and GAC are united in the left-hand side, but they are separated in the right-hand side (LNC+GAC). A square in panel (A) is shown at the higher magnification in panel (B). The inferior end of the GAC extends posteromedially and curled to form the medial crus (E–H). Panels (C–H) were prepared at the same magnification. (A–C) Scale bars=1 mm. IC, inferior concha; NS, nasal septum cartilage; MX, maxilla; VES, vestibulum of the nose; VNO, vomeronasal organ; VO, vomer; SC, sesamoid cartilage.
In late-term fetuses (specimens larger than 216 mm CRL or later than 27 weeks of GA; Figs. 4, 5), a cage-like lateral cartilage was separated from the septal cartilage by sesamoid cartilages in the superior plane. Thus, an articulation with a joint cavity was unlikely between the LNC and septal cartilage in fetuses. An almost 10 week’s “gap” was present between the midterm and late-term specimens. In the gap period, two changes most likely occurred; 1) sesamoid cartilages changed from the round anlagen to the highly wavy bars (Fig. 3H vs. Fig. 5F) and 2) the medial crus of the GAC developed from the antero-inferior end of the GAC (Fig. 3F vs. Fig. 4F). Topographical relation among the LNC, GAC and septal cartilage appeared unchanged (Fig. 3B vs. Fig. 5B).
Fig. 5.
A pair of wavy sesamoid cartilages (SCs) connecting the greater alar cartilage to the nasal septum cartilage (NS). H&E staining. Horizontal sections. A fetus with 230 mm crown-rump length. Panel (A) (or C) displays the most superior (or inferior) plane in the figure. The upper side of each panel corresponds to the anterior side of the head. Squares in panels (A–C) are shown at the higher magnification in panels (D–F), respectively. The lateral nasal cartilage (LNC) and greater alar cartilage (GAC) are still united (LNC+GAC) and they are separated from the NS by wavy SCs (D–F). Panels (A–C) or panels (D–F) were prepared at the same magnification. (A, D) Scale bars=1 mm. IC, inferior concha; VO, vomer.
The LNC and GAC were continuous in the superior plane to form the lateral cartilaginous wall at late-term (Figs. 4A, 5A–C). The sesamoid cartilage appeared small and oval in the superior plane (Fig. 5D, E), but it extended inferiorly to make a long and highly wavy form (Figs. 4B, 5F). The medial crus of the GAC appeared in the antero-inferior side of the septal cartilage. Thus, instead of the septal cartilage, the medial crus provided a medial wall of the nasal vestibulum (Fig. 4E–H). All horizontal sections shown in the figures exhibited planes below the nasal bone. Conversely, at any stages examined, the nasal bone did not exist with sesamoid cartilages in a horizontal section, but it attached to a cage-like nasal capsule in which the future LNC was continuous with the septal cartilage.
A pair of the vomeronasal cartilages sandwiched the posterior end of the septal cartilage and it was adjacent to the ossified vomer and incisive bone (Figs. 2C, E, 3D). The vomeronasal organ was in the anterior side of the cartilage (Figs. 2A, 3A). Overall, the LNC and GAC became separated from the nasal capsule cartilage at 10–12 weeks. At any stages, we did not find a sesamoid cartilage between the LNC and GAC but between the GAC and septal cartilage.
Observations of sagittal sections
Sagittal sections exhibited the septal cartilage widely extending along the supero-inferior axis (Figs. 6, 7). The antero-inferior marginal part of the septal cartilage was near or approaching the nasal vestibulum (Figs. 6A, 7A). Thus, the sagittal sections might provide an impression that not only the LNC but also GAC were continuous with the septal cartilage. However, we had already described that, in levels below the nasal bone, the GAC main part (=lateral crus) was not a median structure like the septal cartilage, but it extended laterally and curled posteromedially to form the medial crus (Fig. 4).
Fig. 6.
The united lateral nasal cartilage (LNC) and greater alar cartilage (GAC) seen in sagittal sections. H&E staining. A fetus with 50 mm crown-rump length. Panels (A) and (C) contain the left and right vomeronasal organs (VNOs), respectively. Panel (B) displays the almost median plane in this specimen. The left-hand side of each panel corresponds to the anterior side of the head. The united lateral nasal and greater alar cartilages continue to the nasal septum cartilage (NS) in superior sites behind the nasal bone (NB). Panels (E) and (F), corresponding to squares in panels (D) and (C), exhibit a candidate anlage (triangle) of medial crus of the GAC. Panels (A–D) or panels (E, F) were prepared at the same magnification. (A) Scale bar=1 mm. (E) Scale bar=0.1 mm. CG, crista galli; CPE, cribriform plate of the ethmoid; FB, frontal bone; VO, vomer; TB, tooth bud.
Fig. 7.
Lateral nasal cartilage looking like an elongation of the nasal septum cartilage (NS). H&E staining. Sagittal sections. A fetus with 274 mm crown-rump length. Panel (A) (or F) displays the most medial (or lateral) plane in the figure. The left-hand side of each panel corresponds to the anterior side of the head. The lateral nasal cartilage (LNC) is identified as an antero-inferior process of the NS (A). Several cartilage bars (arrows in A–C) appear to correspond to the medial crus of the greater alar cartilage (GAC). Small cartilage bars (triangles in B) correspond to a curled superior part of the GAC (insert in C). Insert in panel (D) shows the inferior end of the greater cartilage. Panels (A–F) were prepared at the same magnification. (A) Scale bars=1 mm, 0.1 mm in two inserts. NB, nasal bone; VNC, vomeronasal cartilage; TB, tooth bud; VO, vomer; VES, vestibulum of the nose; CPE, cribriform plate of the ethmoid; FB, frontal bone; NC, nasal capsule cartilage.
A single cartilage plate, corresponding to a united LNC and GAC, appeared to be an antero-inferior process of the septal cartilage (Figs. 6C, 7A) and, at the superior end, it continued to the cribriform plate and crista galli of the cartilaginous ethmoid (Figs. 6A, B, 7F). The GAC was separated from the LNC in late-term fetuses (Fig. 7C, D). The medial crus of GAC was difficult to identify in sagittal sections, but the candidate was identified as a mesenchymal condensation at midterm (Fig. 6E, F) and as several cartilage bars at late-term (Fig. 7A–C). The main part of the GAC was distant from the septal cartilage: both were not seen in a same section. An attachment was unlikely between the medial crus and septal cartilage. Sesamoid cartilages were difficult to identify in sagittal sections possibly due to the small size and wavy shape. Because of no sesamoids, sagittal sections tended to mislead an impression that, throughout the development, the LNC was always continuous with the septal cartilage.
The nasal bone appeared along the LNC at midterm (Fig. 6A–C) and it covered more than half or an almost entire part of LNC at late-term (Fig. 7). The nasal bone extended inferiorly to reach the GAC (Fig. 7E). Thus, the late-term nasal bone was very large relative to the external nasal cartilages. The vomeronasal cartilages were separated from the LNC and GAC by the anterior part of the nasal cavity including the vestibulum (Fig. 7B). Likewise, the vomer did not reach the GAC or the anterior part of the septal cartilage. We did not find a candidate LAC. Finally, Table 2 exhibits a summary of the observations to address the six questions we proposed in the Introduction.
Table 2.
Summary of the observations and answers to six questions in Table 1
| Order | Answer contents |
|---|---|
| A1 | The nasal bone extended inferiorly along the LNC in fetuses. |
| A2 | The LNC was separated from the septal cartilage by sesamoid cartilages. |
| A3 | Sesamoid cartilages might play a buffer role in the postnatal growth. |
| A4 | The GAC, including its medial crus, was separated from the septal cartilage. |
| A5 | The medial crus developed later from the main part of the GAC. |
| A6 | External nasal cartilages were distant from vomeronasal cartilages. |
GAC, greater alar cartilage; LNC, lateral nasal cartilage.
Discussion
We demonstrated that, at late-term, the LNC as well as the GAC including its medial crus was still separated from the septal cartilage. Their connections most likely establish postnatally. Anderson et al. [3] described a wide and tight attachment between the septal cartilage and the GAC medial crus, but we did not find it in fetuses. Sesamoid cartilages were highly wavy and they were not located between the LNC and GAC but between the septal cartilage and GAC. Therefore, anatomy of infant’s external nasal cartilages might be quite different from the adult morphology.
The present observations revealed several unclear points of the external nasal cartilages. The LNC at late-term was small in the supero-inferior axis relative to the nasal bone. Most parts of the infants’ LNC were likely to be covered by the nasal bone and a sliding seemed to occur between the bone and cartilage during the postnatal growth (Q1 in Table 1). The LNC did not make an end-to-end attachment to the septal cartilage and these cartilages were separated by sesamoid cartilages in levels below the nasal bone (Q2). Sesamoid cartilages did not accompany a joint cavity, but the long wavy morphology suggested a buffer role during the postnatal growth. We did not find a sesamoid between the LNC and GAC (Q3). The GAC as well as its medial crus was distant from the septal cartilage (Q4). The medial crus seemed to develop in situ in the inferomedial side of the main part of the GAC, not from the original nasal capsule cartilage (Q5). Because it was not curled in fetuses, the septal cartilage was unable to develop into the medial crus. These answers are summarized in Table 2.
In the adults’ external nose [1, 3], instead of an end-to-end attachment, acutely flexed ends of the LNC, GAC and sesamoid cartilages are interdigitated without any joint cavity interposed in the adults’ external nose [1, 3]. The most striking feature in the present study seemed to be absence of the interdigitated cartilage plates even in late-term fetuses. Indeed, the sesamoids were wavy in fetuses, but the flexed and highly curled morphology seemed to establish during the postnatal growth. Likewise, a postnatal upward sliding of the nasal bone likely occurs along the LNC due to a possible cartilage growth rate much higher than the bone. In addition, the LAC might develop from the GAC after birth. The hypothesized delayed growth of the external nose cartilages seemed to be maintained by the specific matrix substances different from the other cartilage in the head [12].
In references, the anatomy of nasal sesamoid cartilages has been somewhat controversial. According to dissections of 41 fresh cadavers, Ebrahimi et al. [13] reported variations in sesamoid cartilages between the GAC and septal cartilage: a pair of sesamoids in 88% (3×2×0.75 mm at mean) and no sesamoid in 12%. However, Anderson et al. [3] presented a schema in which a pair of sesamoid cartilages are sandwiched by the LNC and GAC. We found sesamoids between the GAC and septal cartilage without attachment to the LNC. Does the sesamoid migrate superficially and superior toward a site between the LNC and GAC after birth? The wavy shape seemed not to allow such a migration. Parts of the nasal capsule cartilage disappear without ossification [11]. Actually, sesamoids are sometimes absent in adults (see above). Therefore, we did not deny a possibility that the fetal sesamoid disappears postnatally and a “new sesamoid” appears. Yamamoto et al. [11] also considered the GAC involved later into the septal cartilage, but the interpretation might be biased by observations of sagittal sections (a limitation of sagittal sections; see the introduction).
The anterior nose including the nasal vestibulum had been called the “internal nasal valve” or “nasal valve region” to emphasize the structure for maintenance of smooth breathing [14, 15]. Since the lateral and medial cruses of the GAC together surround the nasal vestibulum, they are a major skeleton of the valve region. However, the lateral parts of the valve region seem to be dynamically suspended by elastic fiber-rich subcutaneous tissue and striated muscles [16].
The external nasal cartilages were separated from the vomeronasal cartilage by the nasal vestibulum, but the medial crus of GAC existed relatively near the vomeronasal cartilage and vomer. We should correct our previous identification [17] in which a pair of vomeronasal cartilages was regarded as one of alar cartilages. However, the vomeronasal cartilage unlikely develops in association with the vomeronasal organ since they were distant. After birth, the vomeronasal cartilage might ossify to fuse with the vomer.
Footnotes
Author Contributions
Conceptualization: WW, ZWJ, GM. Data acquisition: DG, GM, MY. Data analysis or interpretation: WW, ZWJ, GM, JFRV. Drafting of the manuscript: ZWJ, GM. Funding acquisition: ZWJ. Critical revision of the manuscript: YZ, MY, JFRV. Approval of the final version of the manuscript: all authors.
Conflicts of Interest
No potential conflict of interest relevant to this article was reported.
Funding
This study was supported by a grant from the Doctoral Research Startup Project of Jilin Medical University (JYBS2025033LK) in China.
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