The Laryrigosi~ope
Lippincott Williams & Wilkins, Inc., Philadelphia
0 1999 Thc American Laryngological,
Rhinologicid and Otological Society, Inc.
Effects of Environmental Tobacco Smoke on
Objective Measures of Voice Production
Linda Lee, PhD; Joseph C. Stemple, PhD; Diane Geiger, MA; Rebecca Goldwasser, MA
Okjectiue: The effects of passive smoking on the
voice and laryngeal structures of 20 female passive
smokers and 20 age-matchednonsmokers were exam-
ined.Methods: The voice evaluation consisted of acous-
tic, aerodynamic, and videostroboscopic analyses. Re-
sults: Three passive smokers displayed mild edema or
erythema. Passive smokers had higher mean flow rates
and shorter mean maximum phonation times during
sustained vowels at comfortable, low-, and high-pitch
levels. However, means were only outside normal limits
and significantly Merent from nonsmokers at high
pitch. Variables such as the number of years and hours
per day subjects were exposed to environmental to-
bacco smoke were considered. Concluswm The major-
ity of the variables indicated that vocal fold structure
and function were not adversely altered by exposure to
passive smoke. Differences between these results and
clinical observations are highlighted.
Luryngoscope,109:1531-1534,1999
INTRODUCTION
Passive or involuntary smoking is defined as the expo-
sure of nonsmokers to environmental tobacco smoke (ETS)
and its combustion by-products. ETS is divided into main-
stream smoke, filtered by the lungs and exhaled into the air
by an active smoker, and sidestream smoke, circulated from
smoldering cigarettes, cigars, or pipes.' Because of the low
temperatures of cigarettes left smoldering, sidestream
smoke contains larger concentrations of ammonia, benzene,
carbon monoxide, nicotine, and various other carcinogens
than mainstream smoke.2 In 1990 the Environmental Pro-
tection Agency (EPA) classified sidestream smoke as a class
A (cancer-causing, very hazardous) carcinogen.3 The EPA
report stated that there is no safe threshold for carcinogens
and warned that some proportion of nonsmokers breathing
sidestream smoke would develop tobacco-related cancers.
Research involving passive smokers supports the
EPA warnings. Previous studies have linked ETS with a
~~ .~
From the University of Cincinnati Department of Communication
Sciences nnd llisorders (L.L.), Cincinnati, the Institute for Voice Analysis
and Rehabilitation (J.c.s.), Dayton, the Cincinnati Center for Developmen-
tal Disorders ( 1 1 . ~),Cincinnati,
. and Abilities First (R.G.), Middletown, Ohio.
Editor's Note: This Manuscript was accepted for publication June 14,
1999.
Send ('orrespondence t o Linda Lee, PhD, University of Cincinnati
Department ot'Communication Sciences and Disorders, M.L. 0394, Cincin-
nati, OH 45221-0394, U.S.A. E-mail: linda.lee@uc.edu
Laryngoscope 109: September 1999
variety of disorders in adults, children, and the developing
fetus. Examples include decreased pulmonary function
and respiratory disease, cardiovascular disease, intrauter-
ine growth retardation, early childhood illness (including
sudden infant death), otitis media, and cancers of the
lung, cervix, brain, thyroid and breast (see reviews by
Lesmes and Donofriol and Witschi et al.4 1.
Some side effects of ETS have been linked to changes
in laryngeal structure and function. Reports of throat irrita-
tion and chronic cough are ~ommon.~-ll ETS has also been
significantly correlated with squamous cell head and neck
cancer,lz gastroesophageal reflux,l3 and laryngospasm.14
The deleterious effects of ETS on respiratory and
laryngeal function have been reported. It may be hypoth-
esized that passive smoking may also influence voice pro-
duction, whether directly from the smoke or indirectly
from vocal abuse such as chronic coughing. If passive
smoking affects the voice, the public may need to be edu-
cated. Referrals to otolaryngologists may be warranted;
speech-language pathologists may need to evaluate and
counsel those who are symptomatic. Therefore, the pur-
pose of the present investigation was t o study the effects of
passive smoking on acoustic, aerodynamic, and videostro-
boscopic measures of voice production.
METHODS
Subjects
The subjects were 40 women: 20 passive smokers and 20
nonsmokers, matched for age to within 1 year. The age range was
18 to 49 years (mean = 24.9)for the passive smokers and 18 to 48
years (mean = 25) for the nonsmokers.
Prerequisites for subjects in both groups included no history
of laryngeal pathology or voice therapy and no history of active
smoking. Nonsmokers had never lived with a smoker or worked
in a smoke-filled environment, and rarely encountered tobacco
smoke in any other setting. The number of years the passive
smoking subjects had lived with a smoker ranged from 2 to 38
(mean = 16.8).The number of hours the subjects were exposed to
smoke per day ranged from 2 t o 12 (mean = 4.3).
Procedures
All subjects received both written and verbal explanations of
the procedures used in the investigation. They participated in iden-
tical objective voice evaluations. The evaluation included acoustic,
aerodynamic, and videostroboscopic analyses. Subjects were com-
fortably seated in a quiet room during all phases of data collection.
Lee et al.: Passive Smoking
1531
 Acoustic and aerodynamic analyses during sustained
uowels. Acoustic measures of fundamental frequency, jitter, and
frequency range were obtained using a Visi-Pitch (Kay Elemet-
rics [Lincoln Park, NJ] model 6097). Aerodynamic measures of
phonation volume, airflow rate, and maximum phonation time
were obtained with a Nagashima Phonatory Function Analyzer
(Kelleher Medical, Richmond, VA, model PS 77H).
Acoustic and aerodynamic analyses were performed simulta-
neously. The Visi-Pitch microphone was placed at the end of the
Nagashima air tube, approximately 4 in from the subject’s mouth.
This placement provided a consistently reliable, clear signal and
proved preferable to the signal generated while holding the micro-
phone to the neck.
Data for the acoustic and aerodynamic measures were ob-
tained from sustained vowels la/, Id, and Iul produced at an intensity
level between 75 and 80 dB SPL and at comfortable, high-, and
low-pitch levels. The high and low pitches were defined as the
highest and lowest points in the frequency range in which phonation
could be sustained. If an inappropriate level was chosen, models
were provided to encourage a greater change from modal pitch.
Frequency range. The Visi-Pitch was used to measure the
highest and lowest frequencies in the subject’s total range. Sub-
jects glided from mid-range to either extreme, and were given
multiple trials to obtain their best production.
Videostroboscopic analysis. A rigid scope (Richard Wolf
Medical Instruments Carp., Rosemont, IL) was inserted into the
back of the subject’s oral cavity. Using stroboscopic lighting (Bruel
and Kjaer [Naerum, Denmark1 4914) and a Wolf Saticon Tube
Camera (Richard Wolf Medical Instruments), a videotaped record-
ing was made of the larynx and vocal fold vibration during the
production of the sustained vowel lil a t comfortable pitch. A Panasonic
Recorder (AG-6300) and Color Monitor (BT S 1900N) were used.
Data Analysis
Acoustic and aerodynamic measures. Measures of fun-
damental frequency, jitter, maximum phonation time, flow volume,
and flow rate obtained during the voice analyses were averaged
across the three vowels for each subject. Means and standard devi-
ations were computed. The Multivariate ANOVA (MANOVA) was
performed using programs developed by SPSS-X,Inc. (Chicago, IL).
Three MANOVAs were calculated, one for each pitch level. Homo-
geneity of variance was not problematic because of equal group
sizes.15 Post hoc univariate Analyses of Variance (ANOVAs) were
computed. The main effects consisted of groups (passive smokers vs.
nonsmokers) and the score for each of the five measures.
The lowest and highest frequencies in the frequency range
were determined for each subject. The two extremes were compared
separately (rather than calculating the total frequency range), be-
cause differences between subjects could occur at either end. The dif-
ference scores for the two pitch levels were subjected to an ANOVA.
Videostroboscopic analysis. The videotapes of the strobo-
scopic analyses were evaluated independently by two speech-
language pathologists, each with more than 15 years of experience
in the area of voice disorders and expertise in videostroboscopy. The
subject group was not identified. In cases of disagreement, the
examiners reviewed the tape together until consensus was reached.
Six dimensions of phonatory function were rated: the configu-
ration of glottic closure, the condition of the vocal fold edge, the
amplitude of the vocal fold movement, the mucosal wave, phase
closure, and phase symmetry. Definitions of each of these dimen-
sions are contained in Colton and Casper.I6 A seven-point, equal-
appearing interval scale was used, with 1 representing normal vi-
bration and 7 representing a severe deviation from normal.
Interjudge reliability was determined by rating the video-
stroboscopic evaluations of three randomly chosen subjects a
second time. Ratings were in exact agreement for 19 of the 2 1
variables and within 1 scale point for the remaining two.
Laryngoscope 109: September 1999
1532
A 2 test was calculated for the videostroboscopic ratings. For
each variable, subjects in each group with ratings of 1 (normal
vibration) were compared with those who had ratings greater than
1. Comparisons that were significant a t P < .05 are reported.
The videostroboscopy tapes were also reviewed by an otolar-
yngologist to determine the presence of any laryngeal pathology.
Related Variables. Pearson product correlations were
used to compare the number of years the subject lived with ii
smoker and the number of hours the subject was exposed to
smoke per day with the acoustic and aerodynamic measures.
Significant correlations are reported.
RESULTS
Acoustic and Aerodynamic Analyses During
Sustained Vowels
Results of the MANOVA revealed no significant
group effect for the combined variables at any pitch level
( P > .05).The possibility remains that there were signif-
icant differences between groups on one or more of the five
~ a r i a b l e s . 1Therefore,
~ post hoc univariate analyses of
variance were used to examine the differences between
the two groups with respect to each of the five measures at
the three pitch levels. However, to guard against the pos-
sibility of a type I error, the probability level indicating
significant differences was reduced to .01.
Means and standard deviations for the acoustic and
aerodynamic measures of fundamental frequency, jitter,
phonation volume, flow rate, and maximum phonation time
for the two subject groups are presented in Table I. There
were no significant differences between the passive smokers
and nonsmokers in fundamental frequency, jitter, phonation
volume, or maximum phonation time at any of the pitch levels.
The analyses of variance revealed that there were
significant differences in the flow rates of the passive
smokers and nonsmokers at the high pitch [F(1,38)= 9.92,
P = .003]. The average flow rates of the passive smokers
were higher than those of the nonsmokers at all three
pitches, but these differences reached statistical signifi-
cance only at the highest.
Frequency Range
Means and standard deviations for frequency range
are presented in Table 11. The analyses of variance re-
vealed no significant differences between subject groups
at either end of the frequency range.
Videostroboscopic Analysis
Videostroboscopic evaluation was conducted as the
subjects phonated at comfortable pitch. Slight abnormal-
ities in vocal fold structure were present in three of the 20
passive smokers but in none of the nonsmokers. Two had
mild edema; one had mild erythema. All subjects had
smooth, straight vocal fold edges. Fourteen of the 20 sub-
jects in each subject group demonstrated a posterior glot-
tal chink; one in each group had an anterior chink; the
remaining five had complete closure.
Mean ratings of amplitude of vocal fold movement,
the mucosal wave, phase closure, and phase symmetry are
presented in Table 111. No ratings greater than 4 (of 7)
were assigned to either subject group. Xa analyses re-
Lee et al.: Passive Smoking
 TABLE I
The Acoustic and Aerodynamic Measures of the Passive Smokers and Nonsmokers
- -~
Pitch Level

Comfortable High Low

Fundamental frequency (Hz)
Passive smokers 229 t 31 504 t 79 189 t 25
Nonsmokers 234 2 35 516 t 60 189 t 23
Jitter (%)
Passive smokers 031 t o 1 1 0 54 t 0 18 0 46 2 0 22
Nonsmokers 0332016 0 50 t 0.24 0 40 t 0 15
Phonation volume (ml)
Passive smokers 2,532 t 433 2,579 t 464 2,432 rfr 509
Nonsmokers 2,542 2 532 2,447 t 543 2,480 t 567
Flow rate (ml/s)
Passive smokers 144 ? 41 224 t a5 150 t 74
Nonsmokers 125 2 33 156 t 47 114 rfr 33
Maximum phonation time (s)
Passive smokers 19 t 7 13 2 6 20 t 7
Nonsmokers 22 -+ 6 1725 24 2 9
__
Note Values are mean t SD

vealed that there were no significant between-group dif-
ferences on any of the measures of vocal fold vibration.
Related Variables
The number of years the subject had been exposed t o
passive smoke was negatively correlated with flow rate at
the high pitch level ( r = -0.49, P = ,041. As the number of
years the subject was exposed to smoke increased, flow
rate decreased at this pitch. The number of hours the
subject was exposed to passive smoke per day was not
correlated with any of the variables at any pitch level.
DISCUSSION
Results of the present investigation indicated that
exposure to environmental tobacco smoke may contribute
to some minor changes in vocal fold structure and physi-
ology. Videostroboscopic evaluation revealed mild edema
or erythema in three of the 20 passive smokers. Higher
mean flow rates and shorter mean maximum phonation
times werc observed in this group. However, all means
were within normal limits except for flow rate at high
pitch level, where the mean was greater than 200 mL/s
and differences between the passive smokers and non-
smokers reached statistical significance.
Given the fact that the majority of measures were
within normal limits and that conditions such as edema and
erythema may be due to other forms of vocal misuse or
abuse, we exercise caution in interpretation of the results.
~
TABLE II.
Frequency Range for Passive Smokers and Nonsmokers.
~
Certainly, tissue changes such as edema and erythema are
consistent with some of the previously reported effects of
active smoking. Smoking cigarettes leads to chronic irrita-
tion and an increase in vocal fold mass, especially on the free
vibrating edge of the folds.17J8 Although sidestream smoke
contains less tar than mainstream smoke, it is far from
benign in constitution. Sidestream smoke carries more free
nicotine and higher values of such substances as carbon
monoxide, carbon dioxide, benzene, nitrogen oxide, and am-
monia.l9JO Kuller et al.19 concluded that sidestream smoke,
more toxic and carcinogenic in makeup than mainstream
smoke, would be the more harmful of the two if it were not
diluted by environmental air. ETS has been linked with
laryngeal carcinomas12 and could have caused the more mi-
nor edema and erythema observed in our subjects.
The laryngeal irritation demonstrated by some of the
passive smokers may have contributed to the general pat-
tern of higher mean flow rates and shorter mean maximum
phonation times seen in this group. Hirano21 attributed
greater mean flow rates and decreased maximum phonation
times to swelling of the vocal folds, which typically preclude
complete vocal fold closure. In the present study a significant
correlation indicated that as the number of years subjects
were exposed to ETS increased, flow rate decreased at high
pitch. This finding may not be as contradictory to the general
pattern of higher flow rates found among passive smokers as
it superficially appears. If these speakers had incomplete
closure of the vocal folds at this pitch level, they may have
hyperadducted the laryngeal musculature as a way of com-
pensation. At high pitches, where the folds are already ad-
ducted with greater tension, such hyperadduction would be
expected to decrease flow rate.
Sorensen and Horii”2 showed that the longer the time

Lowest Pitch (Hz) Highest Pitch (Hz)

and the more cigarettes a subject actively smoked, the
Passive smokers 154 t 27 1,130 2 197
greater the changes to the larynx. Based on this finding, we
Nonsmokers 144 t 17 1,152 t 234 hypothesized that the more years and hours per day the
___ - -
~~
~

Nate Values are mean + SD subjects in the present study were exposed t o passive smoke,

Laryngoscope 109: September 1999 Lee et al.: Passive Smoking

1533

Videostroboscopy Ratings’ of the Two Subject Groups.
Amplitude
Passive smokers 1.66 ? 1.06
Nonsmokers 1.25 2 0.40
’1 = normal; 7 severely deviant.
Note: Values are mean t- SD.
the more voice production would be affected. With the excep-
tion of flow rate at high pitch, the correlations did not sup-
port our assumptions. Subjects estimated they were in the
same room with smokers an average of four hours per day. It
is possible that the irritative effects of ETS manifest in some
individuals aRer little exposure and do not change signifi-
cantly over time. Interestingly, every subject stated they had
been exposed more hours per day and in more varied envi-
ronments in the past. However, new awareness of the side-
effects had led family members to begin smoking outside or
in separate rooms, and employment mandates had removed
much of their exposure in the work setting. Finally, other
factors such as the type of ventilation, number of ciga-
rettes smoldering in the room a t one time, o r individual
sensitivity to the by-products may be as important as
the total hours of exposure.
Clinically, we have observed many nonsmoking pa-
tients who are exposed to ETS who demonstrate more of
the characteristics one might expect of a “smoker’s lar-
ynx,” including laryngeal pathologies. We have noted,
however, that many of these patients had been active
smokers in the past. The effect of ETS on a larynx previ-
ously exposed to active smoking is another area needing
investigation. These individuals may be more susceptible
to the side effects of ETS than those like the subjects in
the present study, who face exposure with a healthier
speech-producing system.
Results of the present investigation suggest that en-
vironmental tobacco smoke may contribute to some degen-
erative changes in the larynx, although more subjects
need to be studied before changes in vocal fold physiology
can be attributed directly to it. Fortunately, because of
other serious health implications, numerous public and
private institutions now protect individuals from ETS by
restricting the areas in which smoking is permitted. How-
ever, mere separation of smokers and nonsmokers within
the same air space reduces, but does not eliminate, harm-
ful effects.”:’Additional documentation of the effects of
passive smoking is needed to continue to increase the
awareness of health professionals and the general public
on the hazardous nature of this substance.
ACKNOWLEDGMENT
The authors appreciate the assistance of Drs. Ernest
Weiler and Diya Dutt, who acted as statistical consultants
i n this investigation.
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Laryngoscope 109: September 1999
1534
TABLE 111.
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Wave Phase Closure Symmetry
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1.20 t 0.39 1.10 ? 0.41 1.51 t 1.20
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Lee et al.: Passive Smoking