Structural and ultrastructural study of the anterior portion of the nasal septum and inferior nasal concha.
We used scanning electron microscopy to study and compare the histologic and ultrastructural aspects of the mucosa of the anterior portion of the septum CAPS) and the anterior portion of the inferior concha (APINC) in 10 healthy adults and 10 cadavers. We found that (1) in most cases, the types of epithelium were generally the same in both areas--pseudostratified cylindrical ciliated epithelium with goblet cells (respiratory epithelium), stratified cuboidal epithelium, and stratified squamous nonkeratinized epithelium; (2) the APINC had more respiratory epithelium than the APS; (3) the APS had more squamous epithelium than the APINC; (4) the basement membrane of the APINC was thicker than that of the APS; (5) moderate chronic inflammatory infiltrate was more common in the APINc, and mild infiltrate was more common in the APS; and (6) the APINC had more mucous glands and the APS had more serous glands.
Most published histologic studies of the human nasal mucosa took into consideration only the characteristics of a single isolated anatomic area--that is, either the septum or the inferior concha. Until now, no correlation of the findings between the two areas has been published in the literature.
It has been known since 1895 that the type of epithelium in the nasal mucosa varies by anatomic site, being of a stratified squamous type in the anterior portion of the nasal cavity and of a cylindrical ciliated type in the most posterior portion.  Later it was observed that the epithelium in the nasal mucosa can change as a reaction to exposure to external stimuli.  Among these stimuli are the flow of inspired air, its humidity and temperature, the inhalation of dust particles and chemical products, and trauma. These stimuli can change the type of the epithelium from one that is exclusively pseudostratified cylindrical ciliated with goblet cells (respiratory epithelium) to one that is either stratified cuboidal (epithelium with immature metaplasia), stratified squamous (epithelium with mature metaplasia), or in transition (transition-zone epithelium). 
The type of epithelium is related to the thickness of the basement membrane, which also varies by site. [4,5] The basement membrane is thicker in respiratory epithelium than in squamous epithelium, which suggests the possibility that it acts as a defense barrier for the nasal mucosa. 
In this article, we describe our comparative histologic study of the mucosa of the anterior portion of the septum (APS) and the anterior portion of the inferior concha (APING) with light and scanning electron microscopy. We evaluated not only the types of epithelium and the aspects of the basement membrane, but also the type of inflammatory infiltrate and the distribution of glands in the lamina propria of both areas.
Materials and methods
Our study group consisted of 10 living subjects, aged 18 to 46 years (mean: 28), who had undergone cosmetic rhinoplasty, and 10 cadavers, aged 54 to 76 years at death (mean: 66). None of the cadavers cause of death was related to or had any effect on the nasal cavity or the paranasal sinuses. We used a small forceps to obtain one sample of epithelium from the APS and the APING from each of the 20 subjects. The 40 samples ranged in size from 5 to 10 mm. We defined the APS as the area of the anterior tip of the inferior nasal concha and the APINC as the area 10 mm behind its anterior edge.
Half of each sample was fixed in a 10% formol-Zenker solution for study under light microscopy, and the other half was fixed in a Karnovsky's solution for scanning electron microscopy. The material examined under light microscopy was analyzed to determine the type of epithelium (i.e., one of five possible types), the thickness of the basement membrane (high or low degree), the type of inflammatory infiltrate (mild or moderate), and the type of glands in the lamina propria (serous, mucous, or seromucous). The material examined by scanning electron microscopy was analyzed to correlate the type of epithelium found in this manner with the type found by light microscopy. When more than one type of epithelium was found, which was the case in several samples, we considered only the predominant one.
The criteria for classifying basement membrane thickness and the type of inflammatory infiltrate are subjective, but they are based on a meticulous observation of all sections of each sample and on a comparison among the samples. This is common practice by pathologists. A basement membrane was considered thick only if the thickness was well developed; no morphometric data were obtained. With regard to the presence of glands in the lamina propria, we did not make an actual count; instead we made a cautious and comparative observation of all sections from all samples and took into account the predominant type of gland. Calculations were performed according to the [X.sup.2] test, and a probability level of 0.05 was used to determine statistical significance.
Results Our comparison of the structural arid ultrastructural aspects of the nasal mucosa of the APS and APING revealed the following statistically significant findings:
* Most of the epithelia in the two areas were pseudostratified cylindrical ciliated epithelium with goblet cells (respiratory epithelium), stratified cuboidal epithelium, and stratified squamous nonkeratinized epithelium.
* The APINC contained more respiratory epithelium than the APS.
* The APS contained more squamous epithelium than the APINC.
* The basement membrane of the APINC was thicker than that of the APS.
* The lamina propria of the APINC had a greater amount of moderate chronic inflammation than did the lamina propria of the APS, which had more mild inflammation.
* The APINC had more mucous glands, and the APS had more serous glands.
Epithelium. The percentages of the various types of epithelium found in the 20 samples of mucosa obtained from each of the two areas ([c.sup.2] = 12.67; p[less than]0.05):
* pseudostratified cylindrical ciliated epithelium with goblet cells (respiratory epithelium): APS 20%, APINC 50%
* pseudostratified cylindrical nonciliated epithelium: APS 0%, APINC 10%
* stratified cuboidal epithelium: APS 25%, APINC 35%
* stratified squamous nonkeratinized epithelium: APS 30%, APINC 5%
* stratified squamous keratinized epithelium: APS 25%, APINC 0%
Metaplasia. The differences in the types of epithelium according to the absence or type of metaplasia ([c.sup.2] = 12.05; p[less than]0.05):
* without metaplasia: APS 20%, APINC 50%
* with immature metaplasia: APS 25%, APINC 45%
* with mature metaplasia: APS 55%, APINC 5%
Basement membrane thickness. The differences in the degree of basement membrane thickness ([c.sup.2] = 13.30; p[less than]0.05):
* low degree of thickness: APS 95%, APINC 35%
* high degree of thickness: APS 5%, APINC 65%
Inflammatory infiltrate. The differences between the APS and APINC according to the absence or type of inflammatory infiltrate ([c.sup.2] = 6.31; p[less than]0.05)
* absence of inflammatory infiltrate: APS 5%, APINC 0%
* mild chronic inflammatory infiltrate: APS 90%, APINC 65%
* moderate chronic inflammatory infiltrate: APS 5%, APINC 35%
Glands. The differences in the type and prevalence of glands found in the lamina propria of the APS and APINC ([c.sup.2] = 5.77; p[less than]0.05):
* absence of glands: APS 15%, APINC 0%
* serous glands only: APS 5%, APINC 10%
* equal number of serous and mucous glands: APS 0%, APINC 5%
* preponderance of serous glands: APS 70%, APINC 35%
* preponderance of mucous glands: APS 10%, APINC 50%
Our motivation for undertaking this study was the fact that there has been no report published in the literature that compared the structure of the mucosa of the septum and nasal concha. We endeavored to identify the primary differences and similarities with regard to the constitution of the APS and APINC. We classified our findings according to each of the three analyzed areas of the nasal mucosa: the epithelium, the basement membrane, and the lamina propria.
Epithelium. We found more than one type of epithelium in almost all the samples we analyzed (figure 1). Even so, one type was always predominant, and we considered it to represent the pattern of the area. The most common types were pseudostratified cylindrical ciliated epithelium with goblet cells (figures 2 and 3), stratified cuboidal epithelium (figures 4 and 5), and stratified squamous nonkeratinized epithelium (figures 6 and 7). We also found pseudostratified cylindrical nonciliated epithelium and stratified squamous keratinized epithelium.
Our findings contradict the classic textbook doctrine that only respiratory epithelium is present in the nasal cavity a misconception that has also appeared in some studies published in the literature. [10-2 ]We found respiratory epithelium in 20% of the APS samples and in 50% of the APING samples. Stratified squamous epithelium (keratinized and nonkeratinized combined) was significantly more prevalent in the APS (55%) than in the APINC (5%); stratified squamous keratinized epithelium was present only in the APS.
Several authors have observed that the nasal mucosa becomes altered when it is exposed to external agents. [2,11,13-16] This observation is pertinent to explaining our findings. The mucosa of the APS is more exposed to outside elements, such as air flow and digital trauma. This would also explain the large number of APS samples (25%) that contained stratified squamous keratinized epithelium--the histologic characteristics of which are similar to those of the skin, despite the absence of sudoriferous glands, hair, and hair-erecting muscles and the presence of serous glands (figure 8).
The presence of epithelia other than respiratory epithelium in the APS and APINC has also been observed by other authors. [1,3,6,14-16] This observation is a reflection of the mucosa's s ability to adapt to external stimuli. In histologic analysis, the result of this adaptation phenomenon is seen in the presence of metaplasia and in the differences in the number and distribution of ciliated cells. [17,18] The substitution of one type of epithelium for another is an indication that one type is better adapted to certain circumstances. This metaplastic transformation is more common in areas of the nasal cavity that are more exposed to external agents. As mentioned earlier, only 20% of the APS samples in our study were covered by respiratory epithelium, compared with 50% of the APINC samples (p[less than]0.05). The APS also had a greater amount of epithelium that contained mature metaplasia (55%), as more cells adapted to external agents, than did the APINC (5%) (p[less than]0.05). The extent of the adaptation de pends not on just the direct influence of external factors, but on their duration as well. 
Basement membrane. We analyzed the basement membrane only with respect to the degree of its thickness. Because there were variations in thickness within the samples, we classified each as to its predominant pattern.
Only 5% of the APS samples had a high degree of basement membrane thickness, compared with 65% of the APING samples (p[less than]0.05). A high degree of thickness should not be considered a sign of disease because even completely healthy persons can have fairly thick basement membranes.  Some authors have reported that the basement membrane is often thick in the nasal mucosa,  and others consider basement membrane thickness to be one of the most remarkable histologic characteristics of the respiratory tract.  Some even contend that the basement membrane of the respiratory epithelium is thicker than that of most other epithelia.  Our study revealed that although the thickness of the basement membrane did vary, it was generally thicker in the APING (figure 9) than in the APS (figure 8).
Some authors have reported a correlation between the thickness of the basement membrane and the epithelium of the nasal mucosa. [5,6] They found that the membrane was thicker in the respiratory epithelium and thinner in the stratified squamous keratinized epithelium (figure 8). Our findings are in agreement with those observations. We found a low degree of thickness in 95% of the APS samples, which was proportionate to the high amount of metaplasia we observed in that region (80%). Conversely, we found a high degree of thickness in 65% of the APINC samples, which was similar to the high amount of respiratory epithelium found in that region (50%).
Our findings support the idea that the basement membrane might function as a defense barrier in specific areas of the nasal mucosa. [6,11] There was a high degree of thickness in the APINC, which not only has a greater amount of respiratory epithelium, but is also less adaptable to external agents. On the other hand, there was a low degree of thickness in the APS, where there was more metaplastic epithelium and more adaptability to external stimuli.
Lamina propria. We studied the lamina propria to compare the types of inflammatory infiltrate and the types of glands in the APS and APINC.
Inflammatory infiltrate. Chronic inflammatory infiltrate was present in 39 of the 40 samples; most were mild (figure 10). The only negative sample was obtained from the APS of a healthy adult (figure 8). This finding is in accordance with those of other authors, who considered the presence of mild chronic inflammatory infiltrate to be the normal condition of the nasal mucosa, even in individuals without nasal disease. 
We found a close relationship between the type of inflammatory infiltrate and the type of epithelium. A large quantity (35%) of moderate chronic inflammatory infiltrate was present in the APINC, which, as mentioned, also had a greater amount of respiratory epithelium than did the APS and which was less adaptable to environmental stimuli. The amount of moderate inflammation in the APING samples was seven times higher than that in the APS samples (5%), where the metaplastic epithelium was dominant and in which 90% of the inflammation was mild (figure 10). However, we found no relationship in the lamina propria between the thickness of the basement membrane and the type of inflammatory infiltrate. Although the mucosa of the APINC had a higher degree of basement membrane thickness than did the mucosa of the APS, it also had a higher incidence of moderate inflammation. This finding suggests that the type of epithelium is more important than the thickness of the basement membrane in the defense of the nasal mucosa .
This finding also indicates that the presence of a chronic inflammatory infiltrate is a normal characteristic of the nasal mucosa, as has been reported earlier.  The high incidence of inflammation brings to mind the concept of "physiologic inflammation," and it is probably intimately related to exposure to the flow of inspired air, the influence of environmental agents, and the adaptation phenomenon.
Glands. Most APS and APING samples contained glands. Serous glands were predominant in twice as many APS samples as APING samples (70 and 35%, respectively). On the other hand, mucous glands were predominant in five times as many APINC samples as APS samples (50 and 10%, respectively). Our finding that serous glands are more common in the APS confirms those of other authors. [16,22]
Some studies have shown that the mucous glands are the first glands to degenerate as a result of inflammation.  This could explain why there is a predominance of serous glands during the average lifetime. The idea that the mucous glands are the first to degenerate supports the concept that the predominance of serous glands in the APS, which is more exposed to external agents, represents a normal defense mechanism.
From thc Department of Otorhinolaryngology, College of Medicine, Ciencias Medicas da Santa Casa de Sao Paulo, Brazil (Dr. Augusto, Dr. Filho, and Dr. Dolci), and the Department of Functional Anatomy: Structure and Ultra-structure, Biomedical Sciences Institute, University of Sao Paulo, Brazil (Dr. Konig).
Reprint requests: Arthur Guilherme L.B.S. Augusto, Av. Dr. Altino Arantes, 510 Vila Clementino, CEP 04042-002, Sao Paulo. Brazil. Phone/fax: +55-11-536-9006; e-mail: email@example.com
(1.) Zuckerkandl E. Muqueuse nasale. In: Zuckerkandl E. Anatomie Normale et Pathologique des Fosses Nasales et de Leurs Annexes Pneumatiques. 2nd ed. Paris: G. Masson, 1895:128-35.
(2.) Hilding A. Experimental surgery of the nose and sinuses. Arch Otolaryngol 1932;16:9-18.
(3.) Schall RA. The histology and chronic inflammation of the nasal mucous membrane. Ann Otol Rhinol Laryngol 1933;42:15-38.
(4.) Finek HP. Tissue changes in the nasal mucosa. Preliminary report. Laryngoscope 1927;37:783-97.
(5.) Shambaugh GE. The basement membrane in the mucosa of the upper respiratory passages. Arch Ololaryngol 193l;13:556-69.
(6.) Mansur ES. Alteracoes histoarquiteturais do epitelio de revestimento da mucosa nasal em estado eronico hipertrofico. Revista Brasileira de Otorrinolaringologia 1974;40:273-6.
(7.) Leeson TS, Leeson CR. Sistema respiratorio. In: Leeson TS, Leeson CR. Histologia. 2nd ed. Sao Paulo: Atheneu Editora, 1970:337-60.
(8.) Ham WM. O sistema respiratorio. In: Ham WM. Histologia. 6th ed. Rio de Janeiro: Guanabara Koogan, 1972:714-40.
(9.) Lober PH. Histology and pathology of the nose and sinuses. In: Paparella MM, Shumrick DA. Otolaryngology. 2nd ed. Philadelphia: W.B. Saunders, 1980:470-82.
(10.) Hansel FK. Clinical and histopathologic studies of the nose and sinuses in allergy. J Allergy 1930;l:43-70.
(11.) Jahnke V. Electron microscopic study of the normal and allergic nasal mucosa. Acta Otorhinolaryngol Belg 1978;32:48-55.
(12.) Jafek BW. Ultrastructure of human nasal mucosa. Laryngoscope 1983;93: 1576-99.
(13.) Hollender AR, Fabricant ND. Nasal ionization. Histologic studies in relation to clinical evaluation. Arch Otolaryngol 1938;25:452-68.
(14.) Mygind N, Bretlau P. Scanning electron microscopic studies of the human nasal mucosa in normal persons and in patients with perennial rhinitis. I. Cilia and microvilli. Acta Allergol 1973;28:9-27.
(15.) Boysen M. The surface structure of the human nasal mucosa. I. Ciliated and metaplastic epithelium in normal individuals. A correlated study by scanning/transmission electron and light microscopy. Virchows Arch B Cell Pathol Incl Mol Pathol 1982;40:279-94.
(16.) Baroody F, Naclerio RM. A review of anatomy and physiology of the nose. Presented at Continuing Education Program, American Academy of Otolaryngology--Head and Neck Surgery Foundation; 1990; Alexandria, Va.
(17.) Halama AR, Decreton 5, Bijloos JM, Clement PA. Density of epithelial cells in the normal human nose and the paranasal sinus mucosa. A scanning electron microscopic study. Rhinology 1990;28:25-32.
(18.) Kushnick SD, Pelton-Henrion K, McCormicks A, Kimmelman CP. A scanning electron microscopic study of smoking and actrelated changes in human nasal epithelium. Am J Rhinol 1992;6:185-90.
(19.) Lopes Filho O, Campos CA, Bussolotti Filho I, Dolci JE. Anatomia e fisiologia do nariz e dos seios paranasais. Revista Braslleira de Otorrinolaringologia 1997;64(Suppl 2):l1-31.
(20.) Bambirra S, Lima WT, Colafemina JF, Oliveira JA. Avaliacao clinica e histologica pre e pos-operatoria na associacao da turbinectomia com septoplastia. Revista Brasileira de Otorrinolaringologia 1994;60:195-211.
(21.) Brunner H. Nasal glands. Arch Otolaryngol 1942;35:183-209.
(22.) Malaty HA, Shehata MA, Safi MM. A histologic and histochemical study of the human nasal mucosa in different ages. Alexandria Medical Journal 1970; 15:487-97.
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|Comment:||Structural and ultrastructural study of the anterior portion of the nasal septum and inferior nasal concha.|
|Author:||Konig Jr., Bruno|
|Publication:||Ear, Nose and Throat Journal|
|Date:||May 1, 2001|
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