Eur Arch Otorhinolaryngol (2010) 267:1587–1592
DOI 10.1007/s00405-010-1273-4
LARYNGOLOGY
Laryngeal Wndings and acoustic changes in hubble-bubble
smokers
Abdul-latif Hamdan · Abla Sibai · Dima Oubari ·
Jihad Ashkar · Nabil Fuleihan
Received: 15 October 2009 / Accepted: 30 April 2010 / Published online: 18 May 2010
© Springer-Verlag 2010
Abstract The purpose of our investigation was to evaluate
the laryngeal Wndings and acoustic changes in hubble-
bubble smokers. A total of 42 subjects with history of
hubble-bubble smoking were recruited for this study.
A corresponding group with a history of cigarette smoking
and controls were matched. All subjects underwent laryn-
geal video-endostroboscopic evaluation and acoustic
analysis. In the hubble-bubble smoking group, 61.9% were
males. The average age was 30.02 § 9.48 years and the
average number of years of smoking was 8.09 § 6.45
years. Three subjects had dysphonia at the time of examina-
tion. The incidence of benign lesions of the vocal folds in
the hubble-bubble group was 21.5%, with edema being the
most common at 16.7% followed by cyst at 4.8%. The inci-
dence of laryngeal Wndings was signiWcantly higher in the
hubble-bubble group compared to controls. In the cigarette-
smoking group, the most common Wnding was vocal fold
cyst in 14.8% followed by polyps in 7.4%, and edema,
A. Hamdan (&)
Department of Otolaryngology,
American University of Beirut Medical Center,
P.O. Box: 11-0236, Beirut, Lebanon
e-mail: alhamdan@svclb.com; hamdans2@hotmail.com
A. Sibai
Department of Epidemiology and Population Health,
Faculty of Health Sciences,
American University of Beirut, Beirut, Lebanon
D. Oubari
Specialty Voice Center, Beirut, Lebanon
J. Ashkar · N. Fuleihan
Department of Otolaryngology, Head and Neck Surgery,
American University of Beirut Medical Center,
Beirut, Lebanon
sulcus vocalis and granuloma. These Wndings were not
signiWcantly diVerent from the hubble-bubble group except
for the thick mucus, which was signiWcantly higher in the
latter. There were no signiWcant changes in any of the
acoustic parameters between hubble-bubble smokers and
controls except for the VTI and MPT, which were signiW-
cantly lower in the hubble-bubble group. In comparison
with the cigarette-smoking group, hubble-bubble smokers
had signiWcantly higher Fundamental frequency and habit-
ual pitch (p value 0.042 and 0.008, respectively). The laryn-
geal Wndings in hubble-bubble smokers are comparable to
cigarette smokers. These laryngeal Wndings are not trans-
lated acoustically, as all the acoustic parameters are within
normal range compared to controls.
Keywords Hubble-bubble · Smoking · Stroboscopy ·
Acoustic analysis
Introduction
Smoking is a major health hazard that has been associated
with a variety of diseases related to the respiratory, gastro-
intestinal and other systems of the body. There is a miscon-
ception that modifying the way tobacco is consumed will
reduce its side eVects. Hubble-bubble smoking, also known
as narghile, water pipe, hooka, shisha, goza and meassel, is
a traditional way of smoking that had originated some
400 years ago in Turkey, Iran and India [1]. During recent
years, it has gained more popularity in the Middle East and
has reached Europe and the USA, due to emigration of peo-
ple and exposure of tourists to this kind of smoking. In a
study by Varsano et al. [2], 58% of 9th and 11th grade
students smoked at least once a week, and among the ado-
lescents who smoked, 52% acknowledged that their parents
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knew. The reasons for its widespread use are its ease of
availability, the pleasure it provides and the lack of parental
objection in many communities. As nicotine dependence
seems to develop more in individuals with high levels of
stress, anxiety and depressive symptoms, hubble-bubble
seems to be very common among youngsters with mood
alterations and those under pressure [3].
Narghile consists of tumback, a dark tobacco paste that
is placed on a tray on top of a pipe connected to a glass bot-
tle half Wlled with water. The tobacco is lit by charcoal
embers, and the smoke inhaled is diluted by the water
before entering the lungs (Fig. 1). The combustion of
tobacco leaf yields both gaseous and particulate compo-
nents, such as carbon monoxide, deleterious gases, aerosol
of tar and nicotine particles, all of which are known to be
toxic. Substantial evidences from scientiWc studies concern-
ing the health hazards of hubble-bubble smoking are not
many. Shehade et al. [4] have studied the composition of
the smoke aerosol of the Nargileh water pipe and has
reported an increased concentration of tar and volatile
carcinogens. Sajid et al. [5] have shown that the hazard
secondary to carbon monoxide fraction is as high in hub-
ble-bubble smoking as in cigarette smoking. The size of the Fig. 1 A hubble-bubble
narghile and its burning bowl seems to correlate with the
concentration of carbon monoxide. Singh et al. [6] have included age, gender, number of years of smoking, number
documented that even a single hubble-bubble run results in of hubble-bubble heads smoked per week in the hubble-
increased end expiratory carbon monoxide. Others have bubble smoking group and the number of packs per day in
demonstrated a reduction in lung function tests among nar- cigarette smoking. All subjects were asked whether they
ghile smokers that was attributed to the high levels of had dysphonia at the time of examination. Dysphonia was
superoxide released from leukocytes [7, 8]. Short-term deWned as a change in voice quality perceived by the sub-
eVects on the cardiovascular system included a modest ject himself/herself.
increase in heart rate, systolic blood pressure, diastolic and All subjects underwent laryngeal video-endostrobo-
mean arterial blood pressure [9]. Sukumar et al. [10] have scopic evaluation using the 70° rigid telescope coupled to
shown that rural subjects using hubble-bubble were associ- the Karl Storz Laryngostrobe model 8020 and to a 30 mm
ated with increased cadmium (Cd) in hair and nails. With single chip color Storz endoscopic telecam Dx pal 202320
respect to the incidence of malignant diseases, El Hakim 20. The following parameters were recorded: polyp, cyst,
et al. have shown that hubble-bubble smoking is associated nodules, edema, sulcus vocalis, granuloma, thick mucus,
with a higher rate of lower lip and oral cavity carcinoma, dilated vessels and others, such as leukoplakia or ulcer for-
and Lubin et al. have reported a higher risk for lung cancer mation.
among this group of smokers [11, 12]. The acoustic analysis was performed using the Kay
No study has looked at the eVect of hubble-bubble smok- Elemetric VISI Pitch (Model 3300). The VISI Pitch acoustic
ing on voice. The purpose of our investigation was to analysis works reliably when the acoustic signal contains
evaluate the laryngeal Wndings and acoustic changes in little or no noise and shows a certain amount of periodicity.
hubble-bubble smokers. While the patient was seated in a quiet oYce, the patient’s
vocal signal was recorded directly into the system using a
condenser microphone at a distance of 15 cm from the
Materials and methods mouth. The voice segment chosen was in the middle of a
sustained vowel at the modal register. The following
A total of 30 subjects with a history of hubble-bubble acoustic variables were measured: average fundamental
smoking were recruited for this study. A corresponding frequency, relative average perturbation, shimmer, noise to
group of 27 subjects with history of cigarette smoking and harmonic ratio, voice turbulence index and habitual pitch.
32 controls with no history of smoking matched according The habitual pitch was measured by asking the subject to
to age and gender were also recruited. Demographic data count to ten in a normal voice. The remaining variables

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Eur Arch Otorhinolaryngol (2010) 267:1587–1592 1589

were measured by asking the subject to sustain the vowel/
ah/for 2 s, using the voice quality assessment module of the
VISI Pitch system. The acoustic analysis test was repeated
three times to have a good estimate.
Statistical method
average number of hubble-bubble heads smoked per week
was 7.95. In the cigarette-smoking group, there were 67%
males and the rest were females. The average age was
38.3 § 9.85 years. The average number of years of smok-
ing was 17.4 years. The average number of cigarette packs
smoked per day was 1.4 (see Table 1).

Frequencies, means and standard deviation (SD) were used
to describe the study sample. We assessed diVerences in
vocal symptoms and acoustic analysis parameters between
each pair of the three comparison groups: cigarette smok-
ers, hubble-bubble smokers and controls. Nonparametric
tests, Mann–Whitney U test and Chi-square test were used
for continuous and categorical variables, respectively.
A P value of <0.05 was considered to be signiWcant. All
analyses were conducted using SPSS software.
Results
Demographic data
In the hubble-bubble smoking group, 61.9% were males.
The average age was 30.02 § 9.48 years and the average
number of years of smoking was 8.09 § 6.45 years. The
Laryngeal video-stroboscopic Wndings
The incidence of benign lesions of the vocal folds in the
hubble-bubble group was 21.5% with edema being the
most common at 16.7%, followed by cyst at 4.8%. What
was noticeable in this group was the high incidence of thick
mucus threads between the free edges of the vocal folds in
almost one-fourth of the subjects and the presence of
dilated vessels on the upper lip of the vocal folds in 14.3%
of the cases. The presence of vocal fold edema, thick mucus
and dilated vessels was signiWcantly higher in the hubble-
bubble group compared to controls.
In the cigarette-smoking group, the most common Wnd-
ings were vocal fold cyst in 14.8%, polyps in 7.4% and
edema in 3.7%, followed by sulcus vocalis and granuloma.
These Wndings were not signiWcantly diVerent from the
hubble-bubble group, except for the thick mucus that was
signiWcantly higher in the latter (see Table 2).

Table 1 Demographic data

Cigarette smokers Hubble-bubble smokers Control

Total N 27 42 41
Gender (%)
Male 18 (66.7) 26 (61.9) 28 (68.3)
Female 9 (33.3) 16 (38.1) 13 (31.7)
Age (mean § SD) 38.56 § 9.85 30.02 § 9.48 30.10 § 6.35
Years of smoking (mean § SD) 17.37 § 7.80 8.09 § 6.45
Frequency of packet per day (mean § SD) 1.42 § 0.755
Frequency of head smoked per week (mean § SD) 7.95 § 8.30

Table 2 Laryngeal video-stroboscopic Wndings in hubble-bubble smokers, cigarette smokers and nonsmokers
Nonsmokers Cigarette smoking Hubble-bubble p value (hubble-bubble p value (hubble-bubble
n = 41 (%) n = 27 (%) smoking n = 42 (%) versus nonsmokers) versus cigarette smokers)

Polyps 0.0 7.4 0 – 0.150

Nodules 2.44 0.0 0 1 –
Edema 0 3.7 16.7 0.012 0.136
Cyst 0.0 14.8 4.8 0.494 0.201
Lesions 0.0 0.0 0 – –
Mucus 4.87 0.0 23.8 0.026 0.005
Granuloma 0.0 3.7 0 – 0.391
Varix 0.0 0.0 14.3 0.026 0.075
Sulcus vocalis 0.0 3.7 0 – 0.391

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Table 3 Acoustic Wndings in hubble-bubble smokers, cigarette smokers and nonsmokers

Nonsmokers Cigarette Hubble-bubble p value (hubble- p value
n = 41 smoking n = 27 smoking n = 42 bubble versus (hubble-bubble
nonsmoker) versus
Mean SD Mean SD Mean SD cigarette smoker)

F0 (Hz) (total) 144.5767 41.86703 132.2159 42.28139 154.2967 46.2396 0.389 0.042
Male 118.10 15.78 109.18 17.405 126.026 31.002
Female 201.6 11.15 178.28 39.81 200.236 24.61
RAP % 0.8001 0.51954 0.8581 0.54597 0.8188 0.41396 0.521 0.828
Shimmer % 3.7545 1.87005 2.9890 1.49019 3.1012 1.18641 0.113 0.606
NHR 0.1237 0.02713 0.1159 0.02705 0.1201 0.02829 0.490 0.525
VTI 0.0312 0.01232 0.0280 0.01211 0.0248 0.01042 0.009 0.286
MPT (s) 18.2277 6.17405 15.4167 6.23561 14.9945 5.43493 0.037 0.813
Habitual pitch (Hz) (total) 146.6863 37.5321 127.7198 39.80393 153.2679 42.6775 0.560 0.008
Male 195.2 12.71 106.57 17.02 127.58 30.84
Female 124.15 18.53 170.01 38.92 195.02 19.68

Acoustic analysis correlating with the severity of the histological lesions.

There were no signiWcant changes in any of the acoustic
parameters between hubble-bubble smokers and controls
except for the VTI and MPT, which were signiWcantly
lower in the hubble-bubble group (p value, 0.009 and
0.037, respectively). In comparison with the cigarette-
smoking group, hubble-bubble smokers had signiWcantly
higher fundamental frequency and habitual pitch (p value,
0.042 and 0.008) (see Table 3).
Discussion
Despite the variability in the composition of tobacco used
in hubble-bubble, the aerosol of water pipe smoke has been
shown to consist of a high concentration of carbon monox-
ide, “tar” and heavy metals. Consequently, the adverse
eVects of smoking a hubble-bubble are as dangerous and
similar to smoking cigarettes. These include increased risk
of malignancies, genetic damage, interference with oxida-
tion, impaired pulmonary function, low birth weight, in
addition to infectious diseases resulting from pipe sharing
and the addition of psychoactive drugs to the tobacco [13].
There are scarce scientiWc studies that examine the eVect
of smoking on voice, with many inconsistencies in the
results attributed to methodological constraints and varie-
ties [14–20]. The eVect of smoking is known to be detri-
mental to the mucous membrane and epithelial lining of the
larynx. Besides its irritant eVects and the resultant reduction
in the mucociliary clearance, smoking is considered to be
the main etiological factor in the development of Reinke’s
edema, with the duration of exposure to cigarette smoke
Longer duration of exposure to smoke can result in higher
degrees of histologic damage [21]. Laryngeal tissues when
continuously exposed to smoking may undergo more sig-
niWcant changes in addition to hyperemia, edema and pool-
ing of secretions, including keratinization, hyperplasia and
squamous cell metaplasia. Histological studies have shown
that only 30.6% of smokers have a normal epithelium and
87% have vocal fold thickening; 90% of squamous cell car-
cinoma occur in heavy smokers above the age of 40 years
[22].
In our study, 33.3% of cigarette smokers and 21.5% of
hubble-bubble smokers had abnormal mucosal lining of the
vocal folds. Factors contributing to the development of
these abnormalities include phonotraumatic behavior, per-
sonality factors, airborne irritants, anatomic malformations,
systemic diseases such as laryngopharyngeal reXux and,
among others, smoking. We can assume that hubble-bubble
smokers are more exposed to airborne irritants. More so,
smoking by itself is associated with higher prevalence of
reXux [23]. These factors compounded together can play a
role in the pathogenesis of the laryngeal pathologies
observed in our hubble-bubble group. The lack of data on
reXux in our study unfortunately constrains the above-
mentioned conclusion.
The local irritant eVect of smoking was also evidenced
by the high incidence of mucus threads between the free
edges of the vocal folds and the presence of dilated vessels
in the hubble-bubble group compared to controls. These
Wndings can be attributed to dehydration and excess mucus
concentration on the superWcial layer of the vocal fold.
The edematous changes in the vocal folds secondary to
smoking were evident in both the hubble-bubble and the

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Eur Arch Otorhinolaryngol (2010) 267:1587–1592
cigarette-smoking group. The presence of edema and polyps in
the vocal folds in almost 11% of the cigarette-smoking group
was commensurate with literature, as smoking is consid-
ered among the main etiological factors for the develop-
ment of Reinke’s edema as well as phonotrauma,
laryngopharyngeal reXux and allergy. In the hubble-bubble
group, edema was present in 16.7% of the cases, thus
reXecting a similar eVect of this type of smoking on the
vocal folds, a Wnding that was not signiWcantly diVerent
from the cigarette-smoking group.
Subsequent to these histological changes, lowering of
the vocal pitch and an increase in the perturbation parame-
ters are invariably anticipated. Results by Guimaraes and
Abberton [24] suggested that cigarette smoking had a pitch
lowering eVect for all the speech tasks, although diVerences
did not reach statistical signiWcances. These Wndings were
in partial agreement with other reports by Sorensen and
Horii [14], and Gilbert and Weismer [16]. The eVect of
chronic tobacco usage on voice was also investigated by
Wiskirska et al. in 20 subjects, who had no dysphonia at the
time of examination. Laryngeal videostroboscopic Wndings
were similar to patients with organic dysphonia, and acous-
tic analysis revealed a decrease in the fundamental fre-
quency and an increase in cycle-to-cycle variations in
frequency [25]. In a similar study, reported by Damborenea
et al., where all subjects were mature nondysphonic adults
whose average age was 38 years, the fundamental fre-
quency of the sustained vowel/a/was lower for smokers
than nonsmokers (115 vs. 129 Hz for males, and 185 vs.
201 for females). They have also reported a signiWcantly
higher jitter for smokers without voice complaints com-
pared to nonsmokers for the vowel “ah” [26]. More so,
Murphy and Doyle have documented an increase in the fun-
damental frequency by 18 Hz in two subjects after 40 h of
nonsmoking. The lowering in pitch has been attributed to
the edematous changes often observed in the vocal folds of
smokers [17]. As the vocal folds become thicker secondary
to submucosal swelling, they tend to vibrate slower result-
ing in a lower habitual pitch and fundamental frequency.
An increase in vocal mass also contributes to an increase in
cycle-to-cycle variation in pitch and intensity. The presence
of an increase in the tremor parameters, as reported by
Gonzalez et al., has suggested a neurologic origin for the
presence of dysphonia in cigarette smokers. In our study,
there was a drop in both the fundamental frequency and
habitual pitch among cigarette smokers compared to con-
trols. In the hubble-bubble group, there were no signiWcant
changes in any of the acoustic parameters, particularly in
the F0 and the habitual pitch, compared to controls, except
for VTI and MPT. On the other hand, compared to the ciga-
rette-smoking group, there was a signiWcant drop in the
fundamental frequency and habitual pitch. This Wnding
conWrms the results reported in literature concerning the
1591
eVect of smoking on the pitch and suggests that this eVect
seems to be more accentuated in the cigarette-smoking
group compared to the hubble-bubble group, probably due
to the longer duration of smoking. In this latter, our acous-
tic Wndings, mainly with respect to the habitual pitch and
fundamental frequency, were not commensurate with our
laryngeal endoscopic Wndings, as one would expect a
decrease in the above-mentioned parameters and an
increase in the cycle-to-cycle variation in pitch and inten-
sity with the presence of edema and other Wndings such as
thick mucus. As we know, the determinants of pitch besides
mass are tension, length and Xow. The lack of abnormal
acoustic Wndings may be attributed either to the nonsigniW-
cance of our laryngeal Wndings or the compensation of the
other factors, mainly tension. More so, it can be attributed
to the fact that most of our subjects were nondysphonic at
the time of examination. Having said that, repeating the
same study on subjects with dysphonia and probably a
longer history of smoking may have yielded abnormal
acoustic Wndings.
Conclusions
Hubble-bubble smoking seems to have an eVect on the
vocal folds. Edema is the most important Wnding together
with excessive or thick mucus. These laryngeal Wndings are
not always translated acoustically, as most of the acoustic
parameters are within normal range compared to controls.
Proper awareness to the eVect of this type of hubble-bubble
smoking on the laryngeal mucosa and voice prior to the
onset of dysphonia or the emergence of any lesion is impor-
tant in certain geographic regions or cultures where nargh-
ileh smoking is permissive and misunderstood.
ConXict of interest statement None.
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