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Laryngeal findings and acoustic changes in light cigar smokers.

Abstract

The aim of this prospective study was to look at the laryngeal findings and acoustic changes in light cigar smokers in comparison to nonsmokers, in the setting of a voice clinic. A total of 22 cigar smokers and 19 nonsmokers used as controls were enrolled in the study. Demographic data included age, number of years smoking, number of cigars per week, history of allergy, and history of reflux. The confounding effects of allergy and reflux were accounted for in the control group. Subjects underwent laryngeal endoscopy and acoustic analysis. On laryngeal endoscopy, the most common laryngealfinding was thick mucus. There was no significant difference in the prevalence of any of the laryngeal findings in cigar smokers vs. controls. In comparison with the control group, both the fundamental frequency and habitual pitch were significantly lower in cigar smokers (p value = 0.034 and 0.004, respectively). We conclude that cigar smokers have lower fundamental frequency and habitual pitch compared to nonsmokers.

Introduction

Cigar consumption is rapidly increasing in the United States. It rose by 44.5% from 1993 through 1996. (1) Based on a survey conducted among Massachusetts adults, cigar usage increased dramatically in men aged 18 to 34 years of age between 1993 and 1997-8, in conjunction with national increases in sales and marketing of cigars. (2) In 2013, a randomized survey of 60,000 noninstitutionalized adults >18 years of age regarding the usage of different types of tobacco showed that 12.6% smoked cigars and 2% smoked them daily. (3) This increase is partially due to the perception that cigars are a safe alternative to cigarettes. Cigar smokers are roughly three times as likely as those who do not smoke cigars to believe cigars are a safer alternative to cigarettes. (2) Despite the fact that cigar smoking poses significant risks that lead to welldocumented morbidity and mortality, the perception that it is less harmful than cigarette smoking does not appear to change over time.

Large, prospective cohort studies have strongly supported an association between cigar smoking and mortality from several types of diseases. (4) In a prospective study from 24 British towns with a mean follow-up of 22 years, pipe/cigar smokers showed a significantly higher risk of major coronary heart disease, stroke, diabetes, and cancer when compared with never-smokers. (5) Activation of inflammation and hemostasis may be mechanisms by which cigarette and pipe/cigar smoking increase cardiovascular risk. (6,7)

In a study by Shapiro et al, looking at the association between cigar smoking and death from tobacco-related cancers in a large, prospective cohort of U.S. men, there was an increased risk of death from cancers of the lung, oral cavity, pharynx, larynx, and esophagus.4 Others have also shown that prolonged usage of tobacco products, including cigars, is associated with the development of rectal cancer and increased stomach cancer mortality in men and women. (8,9)

Despite the reports relating cigar smoking to the prevalence of cancer and cardiovascular diseases, no study has looked at the laryngeal endoscopic changes and acoustic characteristics of cigar smokers. Based on a PubMed search using words "voice" and "cigar," we found no previous reports regarding this perspective.

The purpose of our study is to look at the laryngeal findings and acoustic changes in light cigar smokers in comparison to controls. The authors hypothesize that cigar smoking can affect voice and vocal fold mucosa.

Patients and methods

A total of 22 male cigar smokers were recruited for this study after signing the informed consent approved by the Institution Review Board at the American University of Beirut. Demographic data included age, sex, frequency of cigar smoking per week, number of years smoking, history of allergy, and history of reflux. A total of 19 male controls were also included. Tire confounding effects of allergy and reflux were accounted for by having a similar prevalence in both smokers and nonsmokers. All subjects were males above the age of 18 years.

Laryngeal evaluation. All subjects underwent laryngeal videostroboscopic evaluation using a 70[degrees] rigid telescope. The presence of any vocal fold masses (polyps, cysts, nodules, edema, and granulomas), lesions (leukoplakia, erythroplakia), and/or thick mucus or dilated vessels was reported. The presence of mucus was reported when threads of mucus were spread at the free edges of the vocal folds.

Acoustic evaluation. Subjects also underwent acoustic analysis. While the patient was seated in a quiet office, his vocal signal was recorded directly into the system using a condenser microphone at a distance of 15 cm from the mouth. The following acoustic variables were measured: average fundamental frequency, relative average perturbation, shimmer, noise-to-harmonic ratio, voice turbulence index, maximum phonation time, and habitual pitch.

The maximum phonation time was calculated by asking the subject to take a deep breath and sustain phonation for as long as he could. The habitual pitch was measured by asking the subject to count to 10 in a normal voice. The remaining variables were measured by asking the subject to sustain the vowel /ah/ for 2 seconds, using the voice quality assessment module of the Visi-Pitch system (KayPENTAX; Montvale, N.J.). The acoustic analysis test was repeated twice to provide a good estimate.

Statistical method. Frequencies, means, and standard deviation (SD) were used to describe the study sample. We assessed differences in the laryngeal findings and acoustic analysis parameters between the two groups. Nonparametric tests, the Mann-Whitney U test and the chi-square test, were used for continuous and categorical variables, respectively. A p value <0.05 was considered significant. All analysis was conducted using the Statistical Package for the Social Sciences software version 22 (IBM; Armonk, N.Y.).

Results

Demographic data. The cigar-smoking group included 22 males with a mean age of 44.1 [+ or -] 6.3 years, and the control group included 19 males with a mean age of 29.5 [+ or -] 6.7 years. The average number of cigars smoked per week was 11.6 [+ or -] 8.5, and the duration of smoking was approximately 14 years. Five of the 22 (22.7%) cigar smokers vs. 4 of 19 controls (21.1%) had a history of reflux, and 3 of 22 (13.6%) smokers had a history of allergy vs. 3 (15.8%) of the controls (table 1).

Laryngeal findings. The most common laryngeal finding in the cigar-smoking group was the presence of excessive mucus in 7 of 22 (31.8%) subjects. Only 1 (4.5%) subject had vocal fold edema and I had a vocal fold cyst. When cigar smokers were compared with the control group, there was no significant difference in the prevalence of any of the laryngeal findings (table 2).

Acoustic analysis findings. Both the fundamental frequency and habitual pitch were significantly lower in the cigar smokers than in the controls (p values = 0.034 and 0.004, respectively). There was no significant difference in the prevalence of any of the remaining acoustic variables (table 3).

Discussion

Cigarette smoking is known to affect voice. Its carcinogenic and inflammatory effects have been thoroughly reported in the literature. In a study examining the effect of smoking and drinking on histologic changes in laryngeal tissue, metaplasia in the supraglottic region was found to be increased with aging, alcohol consumption, and tobacco usage. (10) There was also a significant difference in the thickness of the epithelium of the supraglottic region and vocal folds in smokers vs. nonsmokers.

In a studyby Dosemeci et al, which examined the risks of laryngeal cancer in relation to subsites among smokers, the highest risks were observed in the supraglottic region of the larynx. (11) In a histologic examination of vocal fold specimens by Muller and Krohn, which examined the frequency of normal squamous epithelium and precancerous lesions, namely dysplasia and carcinoma in situ, the relative frequency of normal epithelium decreased from 83.3% in nonsmokers to 30.6% in heavy smokers, and the incidence of precancerous lesions increased from 4.2% in nonsmokers to 47.2% in heavy smokers. (12)

Although all forms of smoking are harmful, smoking pipes or cigars has been associated with lower exposure to the lethal products of tobacco and lower levels of morbidity and mortality than smoking cigarettes. In fact, in looking at the effects of the type of smoking on biologic indices of tobacco exposure and toxicity, Funck-Brentano et al showed that pipe or cigar smoking was associated with lower exposure to products of tobacco metabolism than cigarette smoking and to an absence of cytochrome P4501A induction, which is believed to be a major pathway activating carcinogens from tobacco smoke. (13) However, in a case-control epidemiologic study conducted to determine the relationship between quantities and types of tobacco and the risk of cancers at various head and neck sites, despite substantial variations in the tobacco-associated risk for each site, cigar smokers experienced excess risks of cancers of the tongue, pharynx, and larynx. (14)

The results of our study are not in accordance with the literature, as there was no significant change, at least endoscopically, in the vocal fold mucosa and no significant difference in the prevalence of any of the laryngeal findings in comparison with controls. There are several reasons that our results do not agree with those from previous reports: the small sample size, the relatively short duration of smoking and, most importantly, our subjects' light smoking (small number of cigars smoked per week). Nevertheless, our results do not mitigate the conclusions from previous studies and should not preclude us from the belief that cigar smoking has an effect on the laryngeal mucosa.

Besides the potential carcinogenic effect of smoking on the laryngeal mucosa, smoking has an irritant and inflammatory effect on the vocal fold mucosa, vessels, and mucociliary clearance. Smoking is considered one of the main etiologic factors in the development of vocal fold edema and polypoid degeneration. Studies have shown that the duration of exposure correlates with histologic changes, with longer years of smoking resulting in more severe edema and polyp formation. (15)

Pechacek et al have reported in their analysis of 306 male cigar and/or pipe smokers that serum levels of thiocyanate--a biological marker of tobacco use that can be detected in the serum or saliva of smokers--were significantly higher in smokers than in nonsmokers but lower than in cigarette smokers. (16) These results were confirmed by other authors, as well, who have demonstrated that this serum level is also related to the amount of product smoke. (17) Thiocyanate levels are significantly higher in smokers than passive and never-smokers, and an increased serum level has been linked to inflammatory reactions leading to pulmonary fibrosis.

Because we did not test serum or salivary thiocyanate levels in our study, we cannot draw any conclusions regarding the presence or absence of significant inflammatory changes in cigar smokers in relation to the extent of their smoking. The results of our study are not in accordance with the hypothesis regarding the effect of cigar smoking on vocal fold mucosa. The inflammatory effect of cigar smoking was not very evident on laryngeal examination; there was no significant difference in the prevalence of vocal fold edema or laryngitis in smokers vs. controls, and only 1 subject had vocal fold edema. Again, this can be attributed to the light smoking in the subjects recruited, to the small sample size, and to the imaging technique used (laryngeal videostroboscopy). High-speed imaging and/or videokymography might be more revealing of subtle mucosal changes and closure patterns in future investigations.

In addition to its inflammatory effect, smoking is also known to decrease the mucociliary clearance of the laryngeal mucosa, resulting in excess mucus secretions and pooling. Brown et al reported a higher prevalence of chronic cough and phlegm (mucus) in cigar and pipe smokers when compared with nonsmokers. (18)

Several studies have also confirmed that allergy has a higher prevalence among smokers compared to nonsmokers, which means that the presence of mucus could be secondary to both allergy and smoking. In a study by Taylor et al, cigarette smoking was found to be associated with small increases in some markers of allergy and that these changes were most likely acquired after the onset of smoking. (19) Likewise, to study the relation between smoking habits, allergy, and IgE values, Zetterstrom et al investigated the adjuvant effect of smoking on IgE antibody production. (20) Their results indicated an increase in IgE antibodies in smokers, which could be due to the damaging effect of smoking on the upper airway mucosa.

In our study, the high prevalence of mucus in cigar smokers cannot be attributed solely to smoking because of the lack of a significant difference between the two groups. The relatively high prevalence in both cigar smokers (31.8%) and controls (31.6%) might be secondary to the confounding effect of allergy that was present in 14 and 15.8%, respectively, of the cases.

With respect to acoustic analysis, studies investigating the vocal changes in smokers have demonstrated a lowering of pitch. Guimaraes reported a decrease in pitch across all speech tasks in smokers, although differences did not reach statistical significance. (21) Damborenea Tajada et al also reported a lower fundamental frequency for the sustained vowel /a/ in nondysphonic smokers, along with an increase in cycle-to-cycle variation in frequency (jitter). (22) Wiskirska-Woznica et al, in a study including 20 nondysphonic smokers, showed a decrease in the fundamental frequency and an increase in jitter. (23)

In our study, the cigar-smoking group also had a significantly lower fundamental frequency and habitual pitch compared to the control group. Hypothetically, this can be attributed to two factors. One factor is an increase in mass with resultant decrease in pitch. The increase in mass can be in the form of a lesion, edema of the vocal fold, or excessive mucus. The laryngeal findings in our study can only partially support this hypothesis in view of the high prevalence of mucus in cigar smokers and the limited vocal fold changes, namely the presence of edema in 1 patient and a cyst in another. Another factor is the possible decrease or alteration in breathing support as evidenced by a reduction the maximum phonation time, even though it is not significant.

In a study using [sup.99m]Tc-labeled sulfur colloid particles to examine the degree to which cigar smokers inhale and the association between self-reported inhalation and observable cigar particle deposition in the lung, results indicated that cigar smoke is inhaled regardless of self-reported noninhalation and smoking history of the subjects. (24) Thus, even though cigar smokers more often than not deny a history of smoke inhalation, as most of our subjects reported (personal communication with the first author), cigar smoke is inhaled and thus affects the respiratory system. Consequently, cigar smokers may have reduced breathing support, which in turn can affect pitch.

Our study is the first to look at the laryngeal findings and acoustic changes in subjects who smoke cigars. Nevertheless, it carries some limitations: one is the lack of perceptual evaluation of the voice quality in subjects who smoke, and another is the limited number of subj ects we were able to recruit for our study.

Despite the limited number of subjects enrolled in our study, our results are in accordance with the hypothesis that cigar smoking affects voice. Cigar smokers are more likely to have a low fundamental frequency and habitual pitch than controls. These findings could represent early symptoms and signs of vocal fold changes not seen on laryngeal videostroboscopy. Videokympgraphy and/or high-speed imaging might be better at detecting subtle glottic changes. The lack of significant vocal fold changes in our study can also be attributed to the small sample size and the light smoking.

In conclusion, the dramatic rise in cigar consumption brings with it the need to promote early-prevention programs and to incorporate cigar smoking into tobacco cessation programs.

References

(1.) Centers for Disease Control and Prevention (CDC). Cigar smoking among teenagers--United States, Massachusetts, and New York, 1996. MMWR Morb Mortal Wkly Rep 1997;46(20):433-40.

(2.) Nyman AL, Taylor TM, Biener L. Trends in cigar smoking and perceptions of health risks among Massachusetts adults. Tob Control 2002;11(suppl 2):ii25-8.

(3.) Agaku IT, King BA, Husten CG, et al. Tobacco product use among adults--United States, 2012-2013. MMWR Morb Mortal Wkly Rep 2014;63(25):542-7.

(4.) Shapiro JA, Jacobs EJ, Thun M J. Cigar smoking in men and risk of death from tobacco-related cancers. J Natl Cancer Inst 2000;92(4):333-7.

(5.) Shaper AG, WannametheeSG, Walker M. Pipeandcigarsmokingand major cardiovascular events, cancer incidence and all-cause mortality in middle-aged British men. Int J Epidemiol 2003;32(5):802-8.

(6.) Wannamethee SG, Lowe GD, Shaper AG. et al. Associations between cigarette smoking, pipe/cigar smoking, and smoking cessation, and haemostatic and inflammatory markers for cardiovascular disease. Eur Heart J 2005;26(17):1765-73.

(7.) Vlachopoulos C, Alexopoulos N, Panagiotakos D, et al. Cigar smoking has an acute detrimental effect on arterial stiffness. Am J Hypertens 2004;17(4):299-303.

(8.) Chao A, Thun MJ, Henley SJ, et al. Cigarette smoking, use of other tobacco products and stomach cancer mortality in US adults: The Cancer Prevention Study II. Int J Cancer 2002;101(4):380-9.

(9.) Sharpe CR, Siemiatycki JA, Rachet BP. The effects of smoking on the risk of colorectal cancer. Dis Colon Rectum 2002;45(8):1041-50.

(10.) Hirabayashi H, Koshii K, Uno K, et al. Laryngeal epithelial changes on effects of smoking and drinking. Auris Nasus Larynx 1990;17(2):105-14.

(11.) Dosemeci M, Gokmen I, Unsal M, et al. Tobacco, alcohol use, and risks of laryngeal and lung cancer by subsite and histologic type in Turkey. Cancer Causes Control 1997;8(5):729-37.

(12.) Muller KM, Krohn BR. Smoking habits and their relationship to precancerous lesions of the larynx. J Cancer Res Clin Oncol 1980;96(2):211-17.

(13.) Funck-Brentano C, Raphael M, Lafontaine M, et al. Effects of type of smoking (pipe, cigars or cigarettes) on biological indices of tobacco exposure and toxicity. Lung Cancer 2006;54(1):11-18.

(14.) Stockwell HG, Lyman GH. Impact of smoking and smokeless tobacco on the risk of cancer of the head and neck. Head Neck Surg 1986;9(2):104-10.

(15.) Vecerina-Volic S, Kovac D, Gulic R. Smokers' edema of the vocal cords [in Croatian], Lijec Vjesn 1997;119(1):1-4.

(16.) Pechacek TF, Folsom AR, de Gaudermaris R, et al. Smoke exposure in pipe and cigar smokers. Serum thiocyanate measures. JAMA 1985;254(23):3330-2.

(17.) Ockene JK, Pechacek TF, Vogt T, Svendsen K. Does switching from cigarettes to pipes or cigars reduce tobacco smoke exposure? Am J Public Health 1987;77(11): 1412-16.

(18.) Brown CA, Woodward M, Tunstall-Pedoe H. Prevalence of chronic cough and phlegm among male cigar and pipe smokers: Results of the Scottish Heart Health Study. Thorax 1993;48(11):1163-7.

(19.) Taylor RG, Gross E, Joyce H, et al. Smoking, allergy, and the differential white blood cell count. Thorax 1985; 40(1):17-22.

(20.) Zetterstrom O, Osterman K, Machado L, Johansson SG. Another smoking hazard: Raised serum IgE concentration and increased risk of occupational allergy. Br Med J (Clin Res Ed) 1981;283(6301):1215-17.

(21.) Guimaraes I. An electrolaryngographic study of dysphonic Portuguese speakers [PhD Dissertation], London, UK: University of London (University College London); 2002.

(22.) Damborenea Tajada J, Fernandez Lieza R, Llorente Arenas E, et al. The effect of tobacco consumption on acoustic voice analysis [in Spanish], Acta Otorrinolaring Esp 1999;50(6):448-52.

(23.) Wiskirska-Woznica B, Obrebowski A, Swidziriski P, et al. Effect of smoking on phonation [in Polish]. Przegl Lek 2004;61(10):1068-70.

(24.) McDonald LJ, Bhatia RS, Hollett PD. Deposition of cigar smoke particles in the lung: Evaluation with ventilation scan using (99m) Tc-labeled sulfur colloid particles. J Nucl Med 2002;43(12):1591-5.

Abdul-latif Hamdan, MD, FACS; Randa Al-Barazi, MD; Jihad Ashkar, MD; Sami Husseini, MD; Alexander Dowli, MD; Nabil Fuleihan, MD

From the Department of Otolaryngology, American University of Beirut Medical Center, Beirut, Lebanon.

Corresponding author: Abdul-latif Hamdan, MD, American University of Beirut Medical Center, PO Box 110236, Beirut, Lebanon. Email: ah77@aub.edu.lb
Table 1. Baseline characteristics of study population and controls

                                   Cigar smokers         Controls
                                     (n = 22)            (n = 19)

Age (years), mean [+ or -] SD    44.1 [+ or -] 6.3   29.5 [+ or -] 6.7
Sex                                    Male                Male
No. cigars smoked/wk,            11.6 [+ or -] 8.5          --
  mean [+ or -] SD)
Years of smoking, mean           14.2 [+ or -] 9.1          --
  [+ or -] SD)
Reflux                                 22.7%               21.1%
Allergy                                14.0%               15.8%

Table 2. Laryngeal findings in cigar smokers and controls

            Cigar smokers   Controls
Findings      (n = 22)      (n = 19)   p Value

Polyps          0.0%          0.0%       --
Nodules         0.0%          0.0%       --
Edema           4.5%          0.0%       --
Cysts           4.5%          0.0%       --
Mucus           31.8%        31.6%      0.617

Table 3. Acoustic findings in cigar smokers and controls

                            Cigar smokers   Controls
                            (n = 22)        (n = 19)

                       Mean     SD     Mean     SD     p Value *

FO (Hz)                111.9   14.9    122.6   14.9      0.034
RAP (%)                0.85    0.61     0.7    0.48      0.677
Shimmer (%)             4.0     2.0     3.4     1.5      0.505
NHR                    0.13    0.043    0.1    0.03      0.592
VTI                    0.03    0.008   0.03    0.01      0.875
MPT (sec)              19.9     8.3    22.0     5.9      0.136
Habitual pitch (Hz)    109.7   15.7    124.3   15.9      0.004

* Significant for p value <0.05

Key: FO = fundamental frequency; RAP = relative average
perturbation; NHR = noise-to-harmonic ratio; VTI = voice
turbulence index; MPT = maximum phonation time.
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Title Annotation:ORIGINAL ARTICLE
Author:Hamdan, Abdul-latif; Barazi, Randa Al-; Ashkar, Jihad; Husseini, Sami; Dowli, Alexander; Fuleihan, N
Publication:Ear, Nose and Throat Journal
Article Type:Report
Date:Jun 1, 2015
Words:3584
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