Deleterious effect of smoking and nasal septal deviation on

Deleterious effect of smoking and nasal septal deviation on
mucociliary clearance and improvement after septoplasty
Murat Karaman, M.D.,* and Arman Tek, M.D.#
ABSTRACT
Objectives: To investigate the effect of septal deviation, septoplasty, and smoking upon nasal mucociliary clearance by using saccharine
test.
Methods: Included in this study were 40 patients (15 women and 25 men) who had septal deviation and septoplasty surgery performed
between March and June 2006. Patients are classified into three groups: group I (n ⫽ 20) nonsmoking patients who had septoplasty surgery,
group II (n ⫽ 20) smoking patients who had septoplasty surgery, and the control (n ⫽ 20) group. None of the control group has nasal
breathing problem or smoking history. For determining preoperative and postoperative nasal mucociliary clearance (MCC) time, a saccharine
test was performed on the patients 1 day before surgery and at the third month of postoperative control.
Results: Preoperative and postoperative nasal MCC time in patients of group I are statistically significantly lower than the group II (p ⬍
0.01). Postoperative MCC time in group I and II is significantly decreased compared with preoperative MCC time, statistically (p ⬍ 0.01).
Preoperative and postoperative MCC time of group I and group II is significantly higher than MCC time of the control group (p ⬍ 0.01).
Conclusion: Nasal septal deviation and smoking deteriorates nasal MCC time and this result can be shown easily with the saccharine test.
Properly performed septoplasty surgery decreases nasal MCC time during the late postoperative period but MCC times are still longer than
normal. The saccharine test can be used for following up the effect of septoplasty upon nasal mucosa.
(Am J Rhinol Allergy 23, 2–7, 2009; doi: 10.2500/ajra.2009.23.3253)
Key words: Nasal mucociliary clearance, postoperative, preoperative, saccharine test, septal deviation, septoplasty, smoking
C
leaning foreign particles over respiratory mucosa and
keeping this mucosa moist are necessary for normal
physiology of the nose. These abilities of respiratory mucosa
depend on effective ciliary activity and renewing of airway
secretions. These are together known as mucociliary activity.
It is known that long-term smoking causes an alteration in
mucociliary clearance (MCC) by decreasing normal cilia population and impairing viscoelasticity of mucus.1
Nasal septal deviation alters nasal physiology by causing
obstruction. In addition, deviation disturbs MCC by increasing mucus secretion, effecting normal ciliary movement, and
causing airway epithelium damage.2,3 The first defense mechanism for the airway is at the nasal fossa mucosa. This mechanism depends on the synergia of mucus and cilia, which
create MCC. Technological improvements have made it possible for us to determine the nasal dynamic phenomena such
as nasal transport function abnormalities within the past 20
years. Surgery is the only curative treatment for nasal septal
deviation. In some literatures it is emphasized that septoplasty effects MCC positively.4,5
Alteration on nasal mucosa can be investigated with the
following mucociliary function studies:
The photometrical method can be used for measuring ciliary movements by evaluation of cilia beat frequency from
randomly selected areas in nasal mucosa. In this method,
ciliary movements can be measured away from hormones,
inflammatory mediators, and stress.6–8
From the *Department of Otorhinolaryngology, Umraniye State Hospital for Research
and Training, Umraniye/İnstanbul and #Department of Otorhinolaryngology, Haydarpasa State Hospital for Research and Training, Üsküdar/İstanbul, Turkey
Address correspondence and reprint requests to Murat Karaman, M.D., Umraniya
State Hospital for Research and Training, Umraniya/İstanbul, Turkey
E-mail address: [email protected]
Copyright © 2009, OceanSide Publications, Inc., U.S.A.
2
The MCC test is used to measure the elimination of inhaled
aerosols.9–11 Saccharine test is one of the methods used for
measuring MCC.12,13
The electron microscope can be used to evaluate histological properties of cilia. The number of united cilia, central
and peripheral microtubulus defect, inner and outer dynein, and ciliary orientation can be investigated in this
method.2
The purpose of this study is to investigate the effect of septal
deviation, septoplasty, and smoking on nasal MCC by using
the saccharine test.
MATERIALS AND METHODS
In total, 40 patients (15 women and 25 men) are included in
this study who underwent septal deviation and septoplasty
surgery between March and June 2006 at the Haydarpasa
Numune Research and Training Hospital. Twenty patients
had a history of smoking (minimal, 1 pack/day; a history of at
least 5 years smoking) and 20 patients did not use cigarettes.
Twenty volunteers were chosen as control group and none of
them had nasal pathologies or smoking history. We did not
encounter any pathologies like septal deviation, rhinosinusitis, nasal polyposis, etc. during the nasal rhinoscopic examination of the control group.
Diagnosis of septal deviation was based on history of patients and complete nasal examination including anterior rhinoscopy and nasal endoscopy (0° rigid endoscope). Patients
with conchal hypertrophy, allergic rhinitis, bacterial or viral
rhinitis, allergic pulmonary disease, asthma, sinusitis, nasal
polyposis, or using drugs (topical or systemic) were excluded
from the study. No medical therapy is given at preoperative
period. For determining preoperative nasal MCC time, sac-
January–February 2009, Vol. 23, No. 1
Table 1 Evaluation of mucociliary clearance (MCC) preoperatively and postoperatively
MCC
Preoperative
Postoperative
§Preop-Postop p
*Values are mean ⫾ SD.
#Student’s t-test.
§Paired sample t-test.
¶p ⬍ 0.01.
Group I (n ⴝ 20)*
22.50 ⫾ 2.70
13.50 ⫾ 2.26
0.001¶
charine testing is performed on the patients 1 day before
surgery.
One milligram per kilogram of pethidine HCL and 0.5 mg
of atropine sulfate are given intramuscularly for premedication and Cottle septoplasty surgery is done under local anesthesia on all patients. Twenty milligrams of lidocaine HC1
(2%) and 0.0125 mg adrenalin within 1 mL known as Jetocaine
(Adeka, Istanbul, Turkey) solution is diluted at a ratio of 1:2
saline physiological solution and used for local anesthesia.
Classic Killian incision was performed and bilateral mucoperichondrium was elevated. After elevation, minimal cartilage excision was made and maxillary crest was excised in all
patients. During the 3-month follow-up period none of the
patients had septal perforation. The patients did not have any
additional nasal surgery (inferior turbinate or sinus) during
septoplasty. At the end of the surgery Merocel packs
(Medtronic, Mystic, CT) were used in 18 patients and nasal
packs were used in 22 patients. Nasal and Merocel packs were
removed at the end of 2nd day after surgery. In addition, oral
antibiotics were applied for 2 days postoperatively. After
nasal packs and Merocel packs were removed saline solution
was ordered three times a day for 2 weeks for irrigation of the
nose and patients were discharged. All patients were called
back for postoperative controls at the 1st week and 1st and 3rd
months. All postoperative patients were evaluated with anterior rhinoscopy (0° endoscopy), secretions were aspirated and
mucosal synechiae were dissected under local anesthesia during each control. Saccharine test was performed on all patients
for determining nasal MCC time at the 3rd month of control
and was done while patients were not using saline solutions
because they may deteriorate the test results.
Saccharine testing was performed preoperatively and postoperatively on 40 patients who underwent septoplasty surgery. In addition, it was performed on 20 patients in the
control group for determining MCC time. Next, average MCC
time was calculated in 40 patients preoperatively and postoperatively in groups 1 and 2, and these average values were
compared to evaluate the effects of smoking and septoplasty
on nasal MCC (Table 1).
Saccharine testing was performed on all patients and the
control group for determining nasal MCC time. Patients were
evaluated according to their average MCC values to determine if there was any significant difference between the
smoking and the nonsmoking group.
MCC Testing
MCC testing was done under normal room temperature
and patients were told to sit comfortably with their heads in
American Journal of Rhinology & Allergy
Group II (n ⴝ 20)*
26.35 ⫾ 1.78
15.80 ⫾ 1.67
0.001¶
p#
0.001¶
0.001¶
a slightly extended position. At first, nasal secretions were
aspirated and then a 1 ⫻ 1 ⫻ 1-mm dimensional (1⁄4 saccharine
tablet) saccharine tablet was positioned to the anterior border
of the medial surface of the inferior turbinate in the deviated
or opposite nasal cavity. Patients were told not to sneeze and
not to bend forward during saccharine test. Also all patients
were requested to gulp for every 30 seconds and tell whenever they felt the taste. The values were rolled up to the
closest half minute and accepted as nasal MCC time.
Statistical Findings
The Statistical Package for Social Sciences (SPSS, Inc., Chicago, IL) for Windows 15.0 program was used for statistical
analysis and paired sample t-test was used for comparison of
the patients in the same group. Data values are expressed as
mean ⫾ SD and Student’s t-test was used for comparison of
the quantitative data between the two groups. One-way
ANOVA test was used for comparison of the quantitative data
between three groups. For the qualitative data comparison
chi-square test was used. Differences were considered as significant when p ⬍ 0.05.
RESULTS
Patients were classified into three groups: group I (n ⫽ 20),
nonsmoking patients who had septoplasty surgery; group II
(n ⫽ 20), smoking patients who had septoplasty surgery; and
control (n ⫽ 20) group. The average age of the patients was
32.48 ⫾ 11.47 years (range, 18–57 years). Twenty-two (36.7%)
of the patients were women and 38 (63.3%) of the patients are
men.
The average age of the 7 female and 13 male patients in
group I was 30.65 years (range, from 18–57 years). The average age of the 8 female and 12 male patients in group II was
33.35 years (range, 18–57 years). The average age of the 7
female and 13 male patients in the control group was 33.45
years (range, 19–53 years; Table 2). None of the volunteers in
the control group were smokers and none had nasal respiratory complaints.
Statistically, there was no significant difference according
to average ages (p ⬎ 0.05) and distribution of gender (p ⬎
0.05) between groups. Preoperative nasal MCC time in patients of group I was statistically significantly lower than the
preoperative nasal MCC time in group II patients (p ⬍ .01).
Postoperative nasal MCC time in patients of group I was
statistically significantly lower than the postoperative nasal
MCC time in group II patients (p ⬍ 0.01).
There was a statistically significant decrease at the postop-
3
Table 2 Evaluation of the groups according to demographic features
Age#
Group I (n ⴝ 20)*
33.35 ⫾ 12.83
Group II (nⴝ 20)*
30.65 ⫾ 10.92
Control (n ⴝ 20)*
33.45 ⫾ 10.91
n (%)
n (%)
7 (35.0)
13 (65.0)
7 (35.0)
13 (65.0)
n (%)
Sex§
Female
8 (40.0)
Male
12 (60.0)
*Values are mean ⫾ SD.
#One-way ANOVA test.
§␹2 test.
p
0.689
0.931
Table 3 Evaluation of preoperative and postoperative mucociliary clearance (MCC) time in group I and the
control group
MCC
Preoperative
Postoperative
*Values are mean ⫾ SD.
#Student’s t-test.
§p ⬍ 0.01.
¶p ⬍ 0.05.
Group I (n ⴝ 20)*
22.50 ⫾ 2.70
13.50 ⫾ 2.26
erative MCC time in group I when compared with preoperative MCC time (p ⬍ 0.01). Also, there was a statistically
significant decrease at the postoperative MCC time in group II
when compared with preoperative MCC time (p ⬍ 0.01).
We compared patients in group I with the control group to
evaluate the effect of septoplasty in nonsmoking patients on
nasal MCC (Table 3). Preoperative MCC time of group I was
significantly higher than MCC time of the control group (p ⬍
0.01). Postoperative MCC time of group I was significantly
higher than MCC time of the control group (p ⫽ 0.001 and p ⬍
0.01). Postoperative MCC time of group I was significantly
higher than MCC time of the control group (p ⫽ 0.039 and p
⬍ 0.05).
We compared nasal MCC time of group II with nasal MCC
time of the control group to determine the effects of both
smoking and nasal septum deviation on nasal MCC and to
observe the improvement of nasal MCC time with septoplasty
surgery (Table 4). Preoperative MCC time of group II was
significantly higher than MCC time of the control group (p ⬍
0.01). Postoperative MCC time of group II was significantly
higher than MCC time of the control group (p ⬍ 0.01).
We compared preoperative MCC time with postoperative
MCC time of groups I and II and the control group to determine the relationship between these values and age (Table 5).
In group I there was a 46% positive correlation between age
and preoperative MCC time and this relationship was statistically significant (r ⫽ 0.460; p ⫽ 0.041; p ⬍ 0.05). Also, there
was a 51.3% positive correlation between age and postoperative MCC time and this relationship was statistically significant (r ⫽ 0.513; p ⫽ 0.021; p ⬍ 0.05). In group II there was an
84.1% positive correlation between age and preoperative
MCC time and this relationship was statistically significant
4
Control (n ⴝ 20)*
12.10 ⫾ 1.86
12.10 ⫾ 1.86
n#
0.001§
0.039¶
(r ⫽ 0.841; p ⫽ 0.001; p ⬍ 0.01). Also, there was a 75.9%
positive correlation between age and postoperative MCC time
and this relationship was statistically significant (r ⫽ 0.759;
p ⫽ 0.001; p ⬍ 0.01). In the control group there was a 64.6%
positive correlation between age and MCC time and this
relationship was statistically significant (r ⫽ 0.646; p ⫽ 0.002;
p ⬍ 0.01).
DISCUSSION
MCC is the most important defense mechanism of nasal
epithelium. Harmful foreign material is held by this mucus
layer and removed from the nasal cavity by ciliary movements.14 MCC can be effected from environmental heat,15
moisture,16,17 partial O2 pressure,18 pH,19 trauma, sulfur dioxide,16,20 formaldehyde, ozone, chlorine,21 smoking,22,23 viral
infections,20 chronic sinusitis,24,25 chronic and allergic rhinitis,26,27 adenoid hypertrophia,28 cystic fibrosis,29 chronic bronchitis,30 septum deviation, surgery, bronchial asthma,31 and
diabetes mellitus.20
Smoking is one of the factors that adversely effects MCC by
changing viscoelasticity of the mucus layer and showing ciliatoxic effects.32,33 Vastag et al.34 studied 71 smoking patients
and found that MCC with chronic bronchitis is worse.34
Ciliary beat frequency and physical properties of the
mucus layer are two important factors that influence the
effectivity of MCC. In mammalians it is known that mucus
secretion of epithelial cells is under hormonal and neural
control. Neural stimulus starts secretion of mucous and this
stimulates ciliary beat mechanically. It has been proven that
increases in mucus secretion stimulate ciliary beat but there
is no proof about direct control of neural and hormonal
January–February 2009, Vol. 23, No. 1
Table 4 Evaluation of preoperative and postoperative mucociliary clearance (MCC) time in group II and the
control group
MCC
Preoperative
Postoperative
*Values are mean ⫾ SD.
#Student’s t-test.
§p ⬍ 0.01.
Group II (n ⴝ 20)*
26.35 ⫾ 1.78
15.80 ⫾ 1.67
Table 5 Relationship between age and nasal
mucociliary clearance (MCC) times
Group I
Preoperative MCC
Postoperative MCC
Group II
Preoperative MCC
Postoperative MCC
Control
MCC
Pearson korelasyon test; *p ⬍ 0.05; #p ⬍ 0.01.
Age (yr)
0.460*
0.513*
0.841#
0.759#
0.646#
stimulus over ciliary beat. In previous studies it has been
shown that heavy smoking, bronchiectasia, asthma, atrophic rhinitis, sinusitis, and nasal polyposis obviously elongates nasal MCC time.10,11,25,35–37
In the study of Stanley et al., 29 smoker and 27 nonsmoker
patients’ nasal MCC times were measured by saccharine test
and compared. They found that mean nasal MCC time of
patients who smoke was 20.8 minutes and mean nasal MCC
time of nonsmoking patients was 11.1 minutes and determined that smoking elongates nasal MCC time. They stated
that smoking regularly decreases cilia number and changes
viscoelastic property of mucus.1 We also investigated the
effects of smoking on MCC in our study. We found that
preoperative and postoperative nasal MCC times in patients
of group I (nonsmoking group) were statistically significantly
lower than in the group II patients (smoking group). This
finding obviously shows the negative effect of smoking on
nasal MCC time in group II.
Preoperative MCC time of group II was significantly higher
than MCC time of the control group. This finding shows that
nasal septum deviation with smoking disturbs nasal MCC.
After septoplasty surgery in properly selected patients the
nasal MCC time decreased at the late postoperative period but
still had longer levels than in the control group (at the 3rd
month). This also shows the negative effect of smoking on
MCC.
James et al.38 investigated the relationship of age and nasal
MCC in a study group aged 11–90 years. They found that as
the patient’s age increases the ciliary beat frequency decreases
and central microtubulus defects become more obvious. Consequently, they stated that over the age of 40 years nasal MCC
time increases. Puchell et al. indicated that mucociliary activity speed in volunteers aged ⬎54 years is lower than younger
volunteers because of mucosal atrophy.39 In the study of
Mortensen et al.40 it was found that there is no statistically
American Journal of Rhinology & Allergy
Control (n ⴝ 20)*
12.10 ⫾ 1.86
12.10 ⫾ 1.86
n#
0.001§
0.001§
significant difference between age and nasal MCC with radioactive studies. In our study in group I there was a positive
correlation between age and preoperative MCC time and the
relationship was statistically significant. In group II there was
a positive correlation between age and preoperative MCC
levels and the relationship was statistically significant. Also,
in the control group there was a positive correlation between
age and nasal MCC levels and the relationship was statistically significant. With these findings, we can say that when
age increases also nasal MCC time prolongs.
In a recent study comparing MCC time of different ethnic
groups with Chinese people, it was found that nasal MCC
time of healthy Chinese people was significantly lower than
other ethnic groups.41 In our study, all of the patients belong
to the same ethnic origin.
Today, two groups of methods are used for measuring
nasal MCC time. First, one contains a direct method such as a
stroboscopic, microcinematographic, or microossilographic
method to observe ciliary movements. The second group is
based on an indirect method, observing the movement of the
mucosal layer from anterior to posterior with various indicators and measuring MCC time. Indirect methods include the
saccharine test and Tc 99m studies. In our study, we preferred
the saccharine test because it can be obtained more easily and
it is more economical than Tc99m. David et al. used saccharine
sky blue to evaluate the MCC time. They judged that if the
septoplasty surgery is successfully performed, nasal MCC
significantly improves. They also found that there is no significant difference in MCC time between obstructed nasal
cavity and the opposite side of the patients with deviated
septum.42 In our study we selected the test side randomly.
Ginzel and Illum43 evaluated 22 patients with deviated
nasal septum as the study group and 60 volunteers as a
control group. In this study, it was found that with properly
performed septoplasty surgery nasal MCC time significantly
decreased. In addition, some animal studies showed that after
sinus surgery MCC time also decreases significantly.10 Shone
et al.44 showed that MCC in nasal cavity improved after septoplasty and endoscopic sinus surgery for nasal polyposis. We
found that preoperative and postoperative nasal MCC time in
group I (nonsmoking group with septal deviation) was statistically significantly higher than the nasal MCC time of the
control group. These findings reveal that nasal obstruction
caused by septal deviation alone disturbs nasal MCC, resulting with longer MCC time. MCC time was decreased at the
late postoperative period, but did not reach the level of the
control group at the 3rd month. These findings correlate with
literature studies.1,41,43
5
In some studies it was determined that nasal MCC was
found disturbed at early postoperative periods of septoplasty.
If basal cells and basal membrane are intact after surgery, the
recovery of nasal mucosa takes 5 days after trauma. If all nasal
mucosa layers are damaged mechanically, it takes 1 week for
stratified epithelium to regenerate, 3 weeks for formation of
new ciliary cells, and at the end of 6th week for total recovery.45 For this reason, we waited for full recovery of nasal
mucosa and evaluated postoperative nasal MCC times at the
3rd month of control.
15.
16.
17.
18.
19.
CONCLUSION
In this study it was detected that nasal septal deviation
and smoking deteriorates nasal MCC time and this result
can be seen easily with the saccharine test. The saccharine
test is a reliable, easy, and harmless method for measuring
nasal MCC time. We showed that properly performed septoplasty surgery decreases nasal MCC time during the late
postoperative period, but MCC times are still longer than
normal.
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