Impact of smoking on nasal mucociliary clearance time in Kano metropolis, Nigeria

Abstract

Background

Mucociliary clearance is an important defense mechanism in human upper and lower respiratory airways. Impairment of this process by certain conditions such as cigarette smoking can predispose to chronic infection and neoplasm of the nose and paranasal sinuses.

Methods

This was a cross‐sectional study conducted in Kano metropolis, Nigeria. Eligible adults were enrolled, a saccharine test was conducted, and the nasal mucociliary clearance time was assessed. Analysis of the result was carried out using Statistical Product and Service Solutions version 23.0.

Results

There were 225 participants categorized into 75 active smokers (33.3%), 74 passive smokers (32.9%), and 76 nonsmokers (33.8%, living in a smoking‐free zone). The age range of the participants was between 18 and 50 years, with a mean age of (31.2 ± 5.6) years. All participants were males. There were 139 (61.8%) of Hausa‐Fulani ethnic group, 24 (10.7%) Yoruba, 18 (8.0%) Igbo, and 44 (19.5%) other ethnic groups. Findings in this study showed that the average mucociliary clearance time among active smokers was prolonged ([15.25 ± 6.20] min) compared to passive ([11.41 ± 4.25] min) and nonsmokers ([9.17 ± 2.76] min) respectively, with a statistical significance (F = 33.59, P < 0.001). Binary logistic regression revealed that the number of cigarettes smoked per day was an independent predictor of prolonged mucociliary clearance time (P = 0.008, odds ratio = 0.44, 95% confidence interval = 0.24–0.80).

Conclusion

Active cigarette smoking is associated with prolonged nasal mucociliary clearance time. The number of cigarette sticks smoked per day was found to be an independent predictor of prolonged mucociliary clearance time.

Impact of smoking on nasal mucociliary clearance time.

INTRODUCTION

The mucociliary system is one of the most important and indispensable mechanisms protecting the airway against ambient microorganisms, foreign particles, and noxious substances. ¹ , ² , ³ , ⁴ The vital part of the mucociliary system is an adequate quantity of mucus, appropriate rhinological qualities, and properly functioning cilia. ⁵ , ⁶

It is imperative to note that several conditions, such as allergic rhinitis, nasal septal deviation, turbinate malformations, nasal polyps, sinonasal tumors, cigarette smoking, and genetic defects of the cilia affect nasal mucociliary clearance. ⁴ , ⁷

Several studies have found that tobacco smoke can alter the nasal mucociliary clearance and can cause an eosinophilic and “allergic‐like” inflammation in the nasal mucosa. ⁶ Some smokers report sensitivity to tobacco smoke manifesting as nose irritation, nasal congestion, rhino rhea, sneezing, and postnasal drip. ⁶ , ⁸ , ⁹

Chemical analytical studies have identified over 3800 compounds in tobacco smoke. ¹⁰ These compounds include carbon monoxide, ammonia, formaldehyde, benzene, nicotine, acrolein, various gases and particles, and an assortment of potentially genotoxic and/or carcinogenic organic compounds. ⁹ , ¹⁰ , ¹¹

Several studies have shown that cigarette smoke and many of its individual components, both gaseous and particulate are associated with numerous structural and functional alterations in the respiratory system, causing increased oxidative stress, airway and lung inflammation, impaired anion transport, and abnormalities in cilia ultrastructure and cilia genesis. ⁸ , ⁹ , ¹² It was also reported that chronic inhalation of cigarette smoke is associated with mucus hypersecretion, pulmonary connective tissue damage, and chronic airflow obstruction. Moreover, cigarette smoking had been established as an important risk factor for nasal, laryngeal, and lung neoplasms. ¹³

Evidence from various literature suggests that mucociliary clearance occurs in the trachea and main bronchi at a similar rate as in the nose. ¹² , ¹⁴ Thus, nasal mucociliary clearance is considered to be representative of pulmonary mucociliary clearance. ¹⁵

Many workers have considered the saccharine test to be a standard technique for the nasal mucociliary clearance measurement, which was described as a simple, inexpensive, readily available, and noninvasive test, providing results similar to those obtained using radioactive particles. ¹³ , ¹⁴ , ¹⁵ , ¹⁶ , ¹⁷ Thus, the saccharine test has a good coefficient of reproducibility in individuals on different occasions.

Studies have shown that normal mucociliary clearance time (MCT) in humans was determined to be 7–15 min using a saccharine test, although some researchers considered any value up to 20 min as normal. ² , ⁴ , ⁷ , ¹⁶

MATERIALS AND METHODS

This was a cross‐sectional study carried out in selected motor parks and within Kano metropolis, Northwestern Nigeria.

Eligibility criteria

Inclusion criteria (for study group)

• 1.Healthy adult smokers (18–50 years).
• 2.An uninterrupted period of active smoking for 1 year.
• 3.Those that consented further participation in the study.

Inclusion criteria (for controls)

• 1.Adult passive smokers.
• 2.Adult nonsmokers.

Exclusion criteria for study group and controls

• 1.History of taste disorders.
• 2.History of nasal surgeries.
• 3.History of ongoing respiratory tract infection.
• 4.Those with nasal polyps/growth.
• 5.Those with gross nasal/septal deformities.
• 6.Those with any nasal symptoms.

Ethical clearance was obtained from the Ethical Review Committee of the Aminu Kano Teaching Hospital (NHREC/21/08/2008/AKTH/EC/2115). In addition, informed written consent was obtained from each study participant. The confidentiality of the participants was strictly maintained throughout the study according to the Helsinki declaration 2013. Eligible adults who met the inclusion criteria were recruited into the study. An interviewer‐based questionnaire was used to obtain their biodata, clinical history, and examination. Anderson's technique of nasal mucociliary clearance assessment was then carried out.

Procedure

Each participant had an anterior rhinoscopy done to identify any gross pathology within the nasal cavity. Participants were asked to clear their nasal cavities of any secretion before the procedure. The nasal cavity tested was selected at random. The procedure entailed inserting sodium saccharin (E954, ISO 9001, USP/BP98, 25 kg/bag marketed by FOODING®) crystal on the anterior end of the inferior turbinate and measuring the average clearance time from the time of insertion to the time when the sweet taste of saccharin was tasted.

A measured piece of saccharin (1‐mm diameter) was placed on the anterior end of the inferior turbinate 1–1.5 cm from the vestibule using crocodile forceps. Participants were instructed to maintain their initial position and were asked to swallow every minute but not to breathe deeply, sniff, or talk during the test. The time from particle placement until the participant reported the first sensation of a sweet taste was measured and expressed as a clearance time in minutes using a stopwatch (Casio Edifice EFR‐544BK‐1A9VUDF, EX 230 Japan).

The participants who did not taste saccharin after 30 min on the the test day were asked to come the next for a repeat test. Those that could not taste on the second day were excluded from the study. Similar procedure was carried out on the control group.

RESULTS

There were 225 participants, categorized into 75 active smokers (33.3%), 74 passive smokers (32.9%), and 76 nonsmokers (33.8%).

The age range of the participants was between 18 and 57 years, with a mean age of (31.2 ± 8.4) years and about 40% of the participants were within the age group of 18–27 years. All participants were males as female active cigarette smokers were difficult to find in the motor parks.

There were 139 (61.8%) Hausa‐Fulani, 24 (10.7%) Yoruba, 18 (8.0%) Igbo, and 44 (19.5%) other ethnic groups, including Marghi, Igala, and Edo. One hundred and thirty participants (57.8%) were single while the rest of the 95 participants (42.2%) were married.

The distribution of the subjects according to occupation revealed: 74 (32.9%) union members, 60 (26.7%) traders/vendors, 30 (13.3%) drivers, and 61 (27.1%) others, including touts, mechanics, and vulcanizers (Table 1).

Table 1.

Distribution of respondents according to sociodemographic status

Variables	Frequency	Percentage (%)
Age (years)
18–27	89	39.6
28–37	82	36.4
38–47	46	20.4
48–57	8	3.6
Gender
Male	225	100.0
Female	0	0
Ethnicity
Hausa‐Fulani	139	61.8
Yoruba	24	10.7
Igbo	18	8.0
Others	44	19.5
Marital status
Unmarried	130	57.8
Married	95	42.2
Occupation
Union members	74	32.9
Traders/vendors	60	26.7
Drivers	30	13.3
Others	61	27.1

Mucociliary clearance time

Prolonged MCT was found in active smokers compared to passive and nonsmokers as shown in Table 2.

Table 2.

Nasal mucociliary clearance time (MCT) in active, passive, and nonsmokers

Group	n	Mean MCT (min)	Range
Active	75	15.25 ± 6.20	5.22–30.17
Passive	74	11.41 ± 4.30	4.19–21.44
Nonsmokers	76	9.17 ± 2.80	3.29–15.2

Note: F statistic determined (F = 33.59; P < 0.001).

Active versus passive (mean difference = 3.87; 95% confidence interval [CI]: 2.141–5.593; P < 0.001).

Active versus nonsmokers (mean difference = 6.10; 95% CI: 4.558–7.642; P < 0.001).

Passive versus nonsmokers (mean difference = 2.23; 95% CI: 1.080–3.388; P = 0.019).

Relationship between MCT and Cigarette sticks/day

The number of cigarette sticks smoked per day was found to be associated with prolonged MCT (P = 0.001) as shown in Table 3 below.

Table 3.

Mucociliary clearance time (MCT) and number of sticks

MCT	Number of cigarette sticks/day
	<20	≥20
Normal	16 (64.0%)	21 (42.0%)
Prolonged	9 (36.0%)	29 (58.0%)
Total	25 (100%)	50 (100%)

Note: χ ² = 24.457; df = 4; P = 0.001.

Regression analysis

The number of cigarette sticks was found to be an independent predictor of prolonged MCT as shown in Table 4.

Table 4.

Binary logistic regression

Predictor	P value	Odds ratio	95% CI
Sticks	0.008	0.44	0.24–0.80a
Duration	0.174	0.70	0.43–1.17

Abbreviation: CI, confidence interval.

^a Have statistical difference.

DISCUSSION

Studies have shown that there were about 1 billion existing smokers in the world and it was estimated that in the next 50 years, 450 million may die because of tobacco‐related diseases. ¹⁸ The increasing prevalence of tobacco use may be because of strong tobacco marketing and a lack of effective tobacco control by governments. ¹⁹ Studies have shown that smoking is a risk factor for many diseases and has been increasingly prevalent in economically developing regions of the world. ²⁰ , ²¹

The Global Adult Tobacco Survey (GATS) conducted in the year 2012 was Nigeria's first official data documenting the prevalence and pattern of adult tobacco use in the country. Until the GATS report, both the government and the civil society in Nigeria have relied on external estimates for policy and advocacy on tobacco. ²²

Reports on cigarette smoking have been found in different age groups ranging from 12 to 69 years; however, studies on adult cigarette smokers mainly reported age groups above 18 years. ³ , ⁵ , ⁷ , ¹³ , ¹⁷ , ²² In this study, the age range of the participants was between 18 and 50 years (mean age of 31.2 ± 8.4). This was similar to the study conducted by Mahakit and Pumhlrun ² on males aged 18–57 years (mean: 30 years). It was also observed that a significant number of the participants (40%) were within the age range of 18–27 years, suggesting a high prevalence of smoking in the young population.

Findings in this study showed that the average MCT between active smokers was (15.25 ± 6.20) min compared to passive smokers (11.41 ± 4.25) min, respectively (Table 2).

The finding was similar to a study done by Baby et al. ²³ whodemonstrated prolonged MCT in smokers compared to healthy control groups, and it was also similar to a study done by Ӧzler ⁴ in Turkey who found longer MCT in active smokers ([15.3 ± 2.34] min) compared to passive smokers ([15.08 ± 3.41] min). Although many workers have not found a significant difference between active and passive smokers (as they consider only smokers and nonsmokers), a study by Yadav et al. ⁵ was able to establish the difference between the two groups (active smokers of [23.08 ± 4.60] min and passive smokers of [20.31 ± 2.51] min), which was similar to findings in our study.

However, other workers reported slightly different results from the one obtained in this study. Utiyama et al. ¹² reported smokers of (17.9 ± 10.1) min while nonsmokers of (8.2 ± 3.1) min. Stanley et al. ¹⁴ reported smokers of (20.1 ± 9.3) min while nonsmokers of (11.1 ± 3.8) min. Karamen and Tek ²⁴ reported smokers of (26.4 ± 1.8) min while nonsmokers of (12.1 ± 1.9) min.

The finding of prolonged MCT was probably due to the ciliotoxic effect of cigarette smoke on the airway mucosa and it was reported that perturbations of the airway epithelial cell barrier induced by cigarette smoke may lead to adverse changes, resulting in airway inflammation. ¹² , ¹³

Studies have shown that an increased amount of cigarettes smoked per day has a multiplier effect on prolonged mucociliary clearance, and the higher the amount of cigarettes smoked, the more the prolonged MCT. ² , ⁴ , ⁵ , ¹⁴

Findings in this study also revealed that there was a strong association between prolonged MCT and increase in the number of cigarettes smoked per day (Table 3). It was observed that out of 38 active smokers with prolonged MCT, 29 (76.3%) smoked ≥20 cigarette sticks per day, while the rest 9 (23.7%) smoked <20 cigarette sticks per day. Binary logistic regression revealed that the number of cigarette sticks smoked per day remained an independent predictor of prolonged MCT (Table 4). The likely explanation was that an increase in the number of cigarettes smoked per day even for a short duration significantly alters the ciliary function of the nasal mucosa.

There was an interesting finding observed in this study. The healthy nonsmoking (third) group considered in this study was selected from a tertiary health institution in Northern Nigeria, which resembled a population studied by Olajuyin et al. ²⁵ in University College Hospital Ibadan, Southern Nigeria. However, the mean MCT of the latter ([13.6 ± 4.6] min) differs significantly from the former ([9.2 ± 2.8] min). The possible explanations were probably due to the difference in the geographical location of the Southern and Northern parts of Nigeria which might have an effect on the mucociliary clearance. It could also be due to genetic differences in taste thresholds as revealed by the two studies. This finding supports the heterogeneity theory of the origin of Nigerians. Although, the aforementioned hypothesis may not have any scientific backup unless a robust study using an objective test instrument (like; electrogustometry) is carried out for clarity.

In conclusion, nasal mucociliary clearance serves an important function of protecting the upper and lower respiratory tract against harmful agents. Active cigarette smoking significantly prolongs nasal MCT as compared to passive smoking. Also, the more the number of cigarette sticks smoked per day the prolonged the MCT.

We recommend that cigarette smoking be discouraged due to the health hazards of tobacco with reference to respiratory diseases and cancers. Legislations on smoking in the future should also be strengthened to control excessive smoking. Robust electrogustometric studies to evaluate the actual taste threshold of Nigerians should be carried out in the future.

AUTHOR CONTRIBUTIONS

Ahmad Mahmud conceived the idea and wrote most part of the manuscript. Abubakar D. Salisu proofread and discussed the manuscript. Emmanuel S. Kolo proofread the manuscript. Muhammad Ghazali Hasheem discussed the manuscript. Nafisatu Bello‐Muhammad wrote the introductory segment. Ahmad R. Tukur designed the study. Yasir J. Nuhu checked and cleaned the data. Rabiu I. Jalo assisted in data analysis.

CONFLICTS OF INTEREST

The authors declare no conflicts of interest.

ETHICS STATEMENT

Ethical clearance was obtained from the Ethical Review Committee of the Aminu Kano Teaching Hospital (NHREC/21/08/2008/AKTH/EC/2115). In addition to this, informed written consent was obtained from each study participant and they were informed about their right to refuse participation or withdraw at any point in the course of the study without fear of any prejudice. The confidentiality of the participants was strictly maintained throughout the study, which was carried out in accordance with the Helsinki declaration 2013. The study was done at no risk or cost to any of the participants and they had the benefit of free nasal examination and information about nasal diseases.

APPENDIX A.

SECTION A: PERSONAL RECORD

• 1.ID no.……………………………………………………………………….
• 2.Address …………………………………………………….……………….
• 3.Age (years)………………………………………………………………….
• 4.Gender: Male [] Female []
• 5.Tribe: Hausa [] Yoruba [] Igbo [] others [] Specify………………………………….
• 6.Marital status: single [] married [] divorced [] widow [] others…….
• 7.Occupation: ……………………………………………………………………………

  SECTION B: SMOKING HABIT

• 8.Number of sticks/day; a. None [] b. 5–10 [] c. 10–20 [] d. above 20 []
• 9.Duration of smoking; a. None [] b. 1–5 years [] c. 6–10 years [] d. above 10 years []
• 10.Reasons for smoking;

  a. pleasure [] b. social acceptance [] c. peer pressure [] d. stress/anxiety []

  SECTION C: CLINICAL HISTORY

• 11.Nasal symptoms;

  a. Sneezing [] b. Nasal discharge [] c. Nasal obstruction []

  d. Nasal itching [] e. Epistaxis [] f. facial pains/headache [] g. None []

• 12.History of nasal allergy/rhinosinusitis; Yes[] No []
• 13.History of Bronchial Asthma; Yes [] No []
• 14.Any systemic illness; Yes [] No []

  SECTION D: RHINOLOGIC FINDINGS

• 15.Patency Normal [] Reduced []
• 16.Nasal mucosa; Pink [] bluish []
• 17.Septum; Central [] Deviated []
• 18.Turbinate; Normal [] Engorged []
• 19.Nasal discharge Present [] Absent []

  SECTION E: SACCHARINE TEST RESULT

• 20.Saccharine test time: (……………minutes)
• 21.Interpretation: tick as appropriate

• a.Positive taste in the nose []
• b.Negative taste in the nose []
• c.Positive taste on the tongue []
• d.Negative taste on the tongue []

Mahmud A, Salisu AD, Kolo ES, et al. Impact of smoking on nasal mucociliary clearance time in Kano metropolis, Nigeria. World J Otorhinolaryngol Head Neck Surg. 2023;9:53‐58. 10.1002/wjo2.61

DATA AVAILABILITY STATEMENT

The data that support the findings of this study are openly available from: (doi. 10.1002/wjo2.61), reference number (WJO261).