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Mucociliary Transport and Histologic Characteristics of the Mucosa of Deviated Nasal Septum
Yong Ju Jang, MD, PhD;
Na-Hye Myong, MD, PhD;
Keun Hwan Park, MD;
Tae Woo Koo, MD;
Han-Gyun Kim, MD
Arch Otolaryngol Head Neck Surg. 2002;128:421-424.
ABSTRACT
Objective To investigate differences in mucociliary clearance, histologic characteristics,
and surface structure of the bilateral nasal septal mucosa in patients with
nasal septal deviation.
Design Mucociliary transport was measured by saccharin clearance time in both
nasal cavities of 20 patients with nasal septal deviation. Their septal mucosae
were taken during septoplasty, and the ciliary population was studied by scanning
electron microscopy. Histologic differences in the lamina propria of septal
mucosae were compared under a light microscope.
Results The concave side showed longer saccharin clearance time than the convex
side and revealed much more severe loss of cilia. Inflammatory cells more
heavily infiltrated the concave side, and seromucinous glands were less densely
distributed.
Conclusion Concave-side septal mucosae have impaired mucociliary transport, presumably
due to ciliary loss, increased inflammation, and decreased density of the
glandular acini.
INTRODUCTION
THE SEVERITY of septal deviations, their location, shape, and complexity
all influence airflow dynamics in the nasal cavity. Thus, in the bilateral
nasal cavities of subjects with nasal septal deviation (NSD), a difference
may occur in the amount of airflow and resistance.1
In response to the difference in airflow dynamics between nasal cavities in
NSD, a compensatory hypertrophy of the nasal mucosa on the side of the nose
opposite the major septal deviation is often found.2
In addition to the compensatory hypertrophy, an impaired mucociliary clearance,
higher incidence of ostiomeatal complex obstruction, and increased incidence
of sinusitis have been reported in subjects with NSD.3-7
Interestingly, sinusitis has been reported to be more severe in the concave
side than in the convex side,5 although a significant
association with ethmoid sinus disease on the convex side has been reported.6 Ostiomeatal complex obstruction and resultant sinusitis
in the direction of septal angulation were attributable to nasal septal deformity.7 However, contralateral ostiomeatal complex obstruction
was suggested to be related to middle-turbinate and lateral-nasal-wall abnormalities,
which appeared with increased frequency on the side opposite the septal deviation.7
Nasal mucociliary clearance is a fundamental function required to maintain
the health and defense of the nose.8 The clinician
should suspect a disorder of mucociliary clearance in a patient who has rhinosinusitis.
In the present study, we hypothesized that the nasal cavities of both sides
in NSD have different mucociliary clearances, and this difference may be responsible
for varying symptoms and increased incidence and severity of sinusitis in
the side opposite the septal deviation. To test this hypothesis, we investigated
the difference in saccharin clearance time (SCT) between nasal cavities. We
also further investigated the difference between the concave- and convex-side
mucosa with respect to anatomical factors such as ciliary population and the
density of inflammatory cells and seromucous glands, which can affect the
mucociliary transport.
PATIENTS AND METHODS
The study was performed with the approval of the Dankook University
Hospital ethics committee, and all the subjects gave written informed consent.
From July 1999 to February 2000, we observed 20 patients (12 men and 8 women),
ranging in age from 21 to 40 years (mean ± SD age, 32.8 ± 15.23
years), who underwent septoplasty for symptomatic NSD, which was diagnosed
by endoscopy and acoustic rhinometry. Thirteen patients showed deviation to
the left side, and the remaining 7 patients showed deviation to the right.
All patients had C-shaped anteroposterior deviation and C-shaped cephalocaudal
septal deviation on endoscopic examination. Patients who had minor spurs or
severe S-shaped septal deviation were excluded. In acoustic rhinometric examination,
all patients revealed a difference of greater than 0.4 cm2 between
nasal cavities in the nondecongested minimal cross-sectional area. Each member
of the control group demonstrated a straight septum on endoscopic examination
and showed a difference in minimal cross-sectional area of less than 0.2 cm2, as determined by acoustic rhinometry. The study population had not
experienced upper respiratory tract infection in the previous 2 months, and
showed normal sinus radiography characterized by the absence of sinus opacity,
mucosal thickening, and air-fluid level in the posteroanterior view and the
Water view. They showed negative results in a skin-prick test using 40 common
inhalant allergens, as determined by a mean wheal size smaller than 2 mm in
diameter and an area less than 25% that of a reference histamine reaction.
During the preoperative evaluation, saccharin tests of both nasal cavities
were conducted separately on consecutive days. A 1-mm-diameter or quarter
fragment of a saccharin tablet was placed on the anterior end of the septal
mucosa, just medial to the anterior end of the inferior turbinate. The patient
was asked to sit quietly, head forward, and not to sniff, sneeze, eat, or
drink. The time taken to the first perception of the sweet taste was recorded.
As a control, the saccharin test was also performed in 15 healthy volunteers
(aged 19-38 years). The control population also had a normal sinus radiograph,
negative results in the skin-prick test, and no history of recent upper respiratory
tract infection.
During the septoplasty, samples of septal mucosae approximately 0.5
x 0.5 cm were taken from the point 2 cm posterior to the nostril and
1.5 cm inferior to the nasal dorsum. Each mucosal sample was divided in 2:
one for scanning electron microscopic examination and the other for light
microscopic examination. For scanning electron microscopic study of the surface
structure, mucosal specimens were immediately immersed in 2.5% glutaraldehyde
in 0.1M cacodyl buffer (pH 7.4) at room temperature. After several hours of
fixation, they were rinsed in 0.1M cacodyl buffer with 0.1M sucrose and postfixed
in 1% osmium tetraxide in 0.1M cacodyl buffer (pH 7.4) at 4°C. The specimens
were dehydrated in graded ethanol series and then dried in a critical point
drier (HCP-2; Hitachi Co, Tokyo, Japan). Samples were coated with gold in
a sputter coater (E 106; Hitachi Co) with 2.5-kV acceleration voltage in an
argon atmosphere with a current of 20 mA for 1 minute. Samples were examined
under a scanning electron microscope (S-2500; Hitachi Co) at 15.0 kV in a
random manner. The degree of ciliary population was graded as 1 (no cilia),
2 (ciliated mucosa occupying less than 30% of the epithelial surface), 3 (ciliated
mucosa occupying 30% to 60% of the surface), or 4 (ciliated mucosa occupying
more than 60% of the epithelial surface). To evaluate the degree of ciliary
population, the proportional area of the ciliated epithelial surface was estimated
by 2 separate investigators on 5 randomly selected mucosal surfaces for each
specimen under x1500 magnification.
For light microscopic examination, the remaining mucosal pieces were
fixed in 10% formalin, embedded in paraffin, and stained with hematoxylin-eosin.
The histologic characteristics observed included the distribution of the nasal
glands and infiltration of inflammatory cells. The number of all types of
inflammatory cells was noted in 5 randomly selected areas of both the subepithelial
layer and the interglandular connective tissue at x400 magnification.
The distribution of nasal glandular tissues was evaluated in the portions
of lamina propria deeper than the subepithelial layer by counting the number
of glandular acini on the randomly selected 5 areas at x400 magnification.
The glandular acini were also classified into serous and mucinous types. The
serous and mucinous glands were characterized by their amphophilic granular
cytoplasms and pale blue or clear cytoplasms, respectively. Light microscopic
examination was also conducted in a blind manner by 2 investigators. The difference
in SCT was statistically tested by 1-way analysis of variance using the PC-SAS
statistical package, version 6.04 (SAS Institute, Cary, NC). The difference
in the degree of ciliary population, number of inflammatory cells, and number
of glandular acini was statistically tested using the t test.
RESULTS
While the mean SCT of the concave-side septal mucosae was significantly
longer than that of the convex nasal cavity in the patients with NSD (P = .02), the SCT was not significantly different between
both nasal cavities in the control group. The SCT in the convex side of patients
with NSD showed no significant difference with those of the septal mucosa
of the right and left side of the normal group, respectively (P>.05) (Table 1).
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Table 1. Mean ± SD Saccharin Clearance Time (SCT) in Bilateral
Nasal Mucosa of Patients With Nasal Septal Deviation (NSD) and Control Subjects
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In scanning electron micrographic examination, the concave-side nasal
mucosa (Figure 1A) showed less dense
ciliary population than the contralateral septal mucosa (Figure 1B). The average score in the grading of ciliary population
was significantly lower in the concave sides, indicating more severe loss
of cilia (P = .005) (Table 2).
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Figure 1. In scanning electron micrographs
of the septal mucosa from each nasal opening in a patient with nasal septal
deviation, the convex side (A) shows sparsely populated cilia (original magnification
x1990), and the concave side (B), densely populated cilia (original
magnification x2180).
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Table 2. Grade Scores of the Ciliary Population Under Scanning Electron
Microscope of Each Nasal Cavity of Patients With Nasal Septal Deviation
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The mean ± SD number of infiltrating inflammatory cells was 52.9
± 4.95 in the convex side of the septal mucosa and 102.5 ± 51.8
in the concave-side septal mucosa (P = .003) (Figure 2). Infiltrating inflammatory cells
were largely lymphocytes, histiocytes, plasma cells, and neutrophils.
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Figure 2. Comparison of the mean ±
SD number of inflammatory cells infiltrating the concave and convex nasal
cavities in patients with nasal septal deviation. Inflammatory cells more
heavily infiltrated the concave side (asterisk indicates P = .003 by the t test).
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The mean ± SD number of submucosal glandular acini was 97.2 ±
16.9 on the convex-side septal mucosa and 66.6 ± 18.7 on the concave-side
septal mucosa, indicating sparse distribution of glandular acini in the concave-side
septal mucosa (Figure 3). Among
the total glandular acini, the respective numbers of mucinous glands and serous
glands also were smaller in the concave-side mucosa (P<.001).
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Figure 3. Comparison of the mean ±
SD numbers of nasal glands in the concave and convex nasal cavities in patients
with nasal septal deviation. There were significantly more nasal glands in
the convex cavity (asterisks indicate P<.001 by
the t test).
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COMMENT
In the present study, the SCT was longer in the concave nasal cavity
than in the convex nasal cavity. Previous investigators have also reported
significantly increased SCT in patients with NSD.3-4
Furthermore, prolonged mucociliary transport (MCT) was normalized 3 months
after septoplasty.3 In contrast, Passali et
al8 found that times for MCT in patients with
NSD were practically identical to those of the control group. This discrepancy
in the results of the previous studies may exist because the MCTs of the bilateral
nasal cavities were not considered independently. However, in our study, we
compared the MCT of the each nasal cavity and found impaired SCT in only the
concave nasal cavity.
In our study, the concave-side septal mucosae revealed more severe loss
of cilia under scanning electron microscopic examination. Ultrastructural
changes of respiratory mucosa can result from acute and chronic infections.9 In experimental study in which one nostril is closed
and the other is open, ciliary loss in the open cavity has been demonstrated.10 Accordingly, in our study, the increased loss of
epithelial cilia in the concave-side septal mucosa might have been caused
by increased airflow.
In the present study, infiltration of inflammatory cells was more prominent
in the concave-side sepal mucosa than in the convex. The exact mechanism for
this occurrence is not understood, but it may be that a spontaneous inflammatory
process not related to allergy or infection may be brought about in the more
open nasal cavity by increased airflow.
In the study by Inagi11 regarding the
histologic changes in the mucous membrane of the human deviated nasal septum,
the mucosa of the concave side collected from 74 cadavers consistently showed
hypertrophic change of the area of mucous glands and the thickness of the
mucoperiosteum. However, in our study, the distribution of seromucinous glands
was less compact in the concave-side septal mucosa than on the convex side.
The different result regarding the distribution of nasal glandular tissue
between the 2 studies may result from the different study populations. In
our study, the study materials were septal mucosa taken from symptomatic living
human subjects with NSD. Thus, our result may better represent the true histologic
features of subjects with NSD complaining of stuffy nose that necessitates
surgical treatment. As for the decreased distribution of the glandular tissue
in our study, it is possible that a chronic inflammatory process of the concave-side
septal mucosa, as demonstrated in our study as an increased infiltration of
inflammatory cells, may lead to stromal proliferation and fibrosis of the
lamina propria, resulting in relative paucity of the glandular acini.
The MCT represents the first barrier of the nasal fossae and paranasal
sinuses against various biological and physical insults. Differences in MCT
rates between different sites in the nose depend on ciliary beat frequency,
density of the ciliary population, length of the cilia, and mucus quality.12-13 The results of our study, which revealed
impaired MCT in the concave nasal cavity, can certainly be explained by the
decreased ciliary population on the ipsilateral side, indicating a loss of
mucociliary machinery. Additionally, a changed property of mucus covering
the epithelium that can result from increased inflammatory infiltrates and
reduced distribution of glandular tissue (not examined in our study) might
have contributed to the impaired MCT in the concave-side septal mucosa.
In conclusion, the results of our study suggest that NSD is not a simple
affliction resulting only in a mechanical alteration of nasal airflow in the
nasal cavity, but a more complex disease process presenting with impaired
mucociliary clearance in the concave-side mucosa that can predispose a patient
to increased incidence and severity of sinusitis in the side opposite the
NSD. The results of this study also indicate that the concave-side septal
mucosa has impaired MCT compared with that of the convex side, probably due
to ciliary loss, increased inflammation, and decreased density of the glandular
acini.
AUTHOR INFORMATION
Accepted for publication October 2, 2001.
Corresponding author and reprints: Han-Gyun Kim, MD, Department of
Otolaryngology, Dankook University College of Medicine, Anseo-Dong 29, Cheonan-City,
Choongnam-Do, Korea 330-714 (e-mail: hgkim99{at}chollian.net).
From the Departments of Otolaryngology (Drs Jang, Park, Koo, and Kim)
and Histopathology (Dr Myong), Dankook University College of Medicine, Cheonan,
Korea.
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