The Laryngoscope

C 2015 The American Laryngological,

V
Rhinological and Otological Society, Inc.

Vocal Fold Varices and Risk of Hemorrhage

Christopher Guan-Zhong Tang, MD; G€

ulce Askin, MPH; Paul J. Christos, DrPH, MS; Lucian Sulica, MD

Objectives/Hypothesis: To establish risk of hemorrhage in patients with varices compared to those without, determine
additional risk factors, and make evidence-based treatment recommendations.
Study Design: Retrospective cohort study.
Methods: Patients who were vocal performers presenting for care during a 24-month period were analyzed to deter-
mine incidence of hemorrhage. Patients with varices were compared to those without. Demographic information and examina-
tion findings (presence, location, character, and size of varices; presence of mucosal lesions or paresis) were analyzed to
determine predictors of hemorrhage.
Results: A total of 513 patients (60.4% female, mean age 36.6 years 6 13.95 years) were evaluated; 14 patients pre-
senting with hemorrhage were excluded. One hundred and twelve (22.4%) patients had varices; 387 (77.6%) did not. The
rate of hemorrhage in patients with varices was 2.68% at 12 months compared to 0.8% in patients without. Cox proportional
hazard regression analysis revealed a hazard ratio of 10.1 for patients with varix developing hemorrhage compared to non-
varix patients (P < 0.0001). The incidence rate of hemorrhage was 3.3 cases per 1,000 person-months for varix patients com-
pared to 0.5 cases per 1,000 person-months in the nonvarix group. There was no significant difference in the incidence of
paresis, mucosal lesions, location of varix (left or right side; medial or lateral), or varix morphology (pinpoint, linear, lake)
between patients who hemorrhaged and those that did not.
Conclusion: The presence of varices increases the risk of hemorrhage. Varix patients had 10 times the rate of hemor-
rhage compared to nonvarix patients, although the overall incidence is low. This data may be used to inform treatment of
patients with varices.
Key Words: Vocal fold hemorrhage, varix, phonotrauma, performing voice, larynx.
Level of Evidence: 4.
Laryngoscope, 126:1163–1168, 2016

INTRODUCTION Vasculature of the lamina propria is arranged to

Vocal fold hemorrhage is an acute phonotraumatic
injury caused by rupture of blood vessels of the lamina
propria. The ensuing dysphonia is typically brisk in
onset, caused by changes in the mass and rheologic
properties of vocal fold tissue resulting from diffusion of
blood through low-resistance tissue of the lamina prop-
ria. Both the rapid onset of the dysphonia, as well as the
ominous appearance of the submucosal ecchymosis,
make the injury dramatic in presentation and the source
of considerable anxiety to patients, particularly vocal
performers.
From the New York Center for Voice and Swallowing Disorders
(C.G-Z.T.), the Sean Parker Institute for the Voice, Department of Otolar-
yngology–Head and Neck Surgery (C.G-Z.T., L.S.), and the Division of Bio-
statistics and Epidemiology, Department of Healthcare Policy and
Research (G.A., P.J.C.), Weill Cornell Medical College, New York, New
York, U.S.A.
Editor’s Note: This Manuscript was accepted for publication
September 15, 2015.
Presented at the 2015 American Laryngological Annual Meeting,
Boston, Massachusetts, U.S.A, April 22, 2015.
Sources of support: P.J.C. and G.A. were partially supported by the
following grant: Clinical and Translational Science Center at Weill Cor-
nell Medical College (UL1-TR000457-06). The authors have no other
funding, financial relationships, or conflicts of interest to disclose.
Send Correspondence to Christopher G. Tang, MD, Department of
Head and Neck Surgery. Kaiser Permanente Medical Center San Fran-
cisco, 450 6th Ave. 2nd Floor, San Francisco, CA 94118. E-mail:
Christopher.G.Tang@kp.org
DOI: 10.1002/lary.25727
withstand the stresses of its environment. Vessels course
in a longitudinal direction to minimize inertial stress
and do not anastomose with those in deeper layers so as
to reduce vulnerability to shear.1 Endothelial cells are
surrounded by an extensive concentric lamellate base-
ment membrane and are reinforced with intracellular fil-
aments to protect against high mechanical vessel wall
stress.1,2 Even so, phonatory vibration can produce
forces sufficient to tear these structures, resulting in
bleeding within the lamina propria. Varices, or abnor-
mally dilated vessel segments, are generally considered
to be especially fragile and prone to rupture.
Several articles describe excision or ablation of
vocal fold varices using various techniques.3–7 The
notion that varices are to be addressed surgically
appears to have evolved despite the absence of funda-
mental data regarding incidence of vocal fold hemor-
rhage and the additional risk, if any, related to the
presence of varices. Not only does this make evaluation
of the efficacy of such an intervention impossible, it also
makes it impossible to weigh the risk of hemorrhage
against the risk of intervention and advise the patient
accordingly.
This study is undertaken to 1) determine the rate
of hemorrhage in patients with varix during the study
period; 2) establish the risk of hemorrhage in these
patients relative to that in patients without varix;

Laryngoscope 126: May 2016 Tang et al.: Vocal Fold Varices and Hemorrhage
1163

Fig. 1. Two pinpoint varices of the right vocal fold. One is at the
midpoint on the vibratory margin, and the other on the medial half
of the superior surface of the vocal fold, posterolateral to the first.
and 3) arrive at an evidence-based recommendation
regarding surgical intervention for vocal fold varices.
MATERIALS AND METHODS
This study was approved by the institutional review board
of Weill Cornell Medical College. Medical records of all patients
presenting for care to a university voice center during a contin-
uous 24-month period were reviewed. The time period was
selected so that a minimum of 1 year would have elapsed after
the patient visit at the time of the record review. Patients pre-
senting with hemorrhage were excluded. To homogenize the
sample both demographically and with respect to vocal demand,
the study population was restricted to vocal performers, defined
as patients whose principal professional activity is public vocal
performance. In practice, this included singers across several
genres of singing, actors, and students if their principal field of
study was vocal performance. Avocational vocalists who derived
their livelihood from a nonperforming activity were excluded.
Schoolteachers, exercise instructors, salespeople, and other pro-
fessions who are often included within the rubric of professional
(as opposed to performing) voice users were similarly excluded.
Patients who had previously been evaluated and came in for
Fig. 2. Long linear varix on medial half of the superior surface of
the left vocal fold.
Laryngoscope 126: May 2016
1164
follow-up visits during the study period were considered to
enter the study at their initial visit.
Demographic and professional information was obtained
via chart review. The initial stroboscopic examination (video
and audio) for each patient was reviewed by the authors,
who were blinded to the original documentation, to deter-
mine the presence, location, character, and size of varices. In
addition, the presence of mucosal lesions and vocal fold pare-
sis was recorded. The occurrence of hemorrhage was deter-
mined by a review of the medical record subsequent to the
principal visit, cross-referenced with the senior author’s (L.S)
database.
Varices were defined as dilated, tortuous, and/or elongated
blood vessels arising from the microcirculation of the vocal fold,
as characterized by Postma et al.8 Varices were categorized as
pinpoint, linear, or vascular lakes based on their appearance.
Pinpoint varices were small, focal, approximately circular dila-
tations (Fig. 1). Linear varices described longer segments of
dilated vessel (Figs. 2 and 3). A vascular lake had a diameter
that is at least twice as large as the diameter of a normally
engorged blood vessel (Fig. 3). Patients with multiple varices
had each varix recorded.
The location of the varix was described by laterality and
location on the vocal fold. Laterality is self-explanatory; location
was categorized as vibratory margin, medial, or lateral. Vibratory
margin lesions were on the contact surface of the vocal fold (Fig.
1). Because these were occasionally below the upper lip of the
glottis, sometimes they could only be seen on eversion of the
leading edge of the vocal fold during phonation. Medial lesions
were determined to be on the superior surface of the vocal fold,
on the medial side of a line halfway between the vibratory mar-
gin and the superior arcuate line delineating the vocal fold
proper from the ventricle (Figs. 1 and 2), whereas lateral lesions
were determined to be on the lateral half of the line (Fig. 3).
Mucosal lesions included cysts, polyps, pseudocysts, sul-
cus, and scar, as well as less clearly defined mucosal change at
the vibratory margin. These were considered as a group and
determined simply to be present or absent. Paresis was identi-
fied clinically based on the presence of specific findings. In
order of importance, these were 1) unilateral atrophy; 2) unilat-
eral ventricular fold hyperfunction; 3) presence of a contact
lesion; 4) impaired adduction; 5) phase difference/asymmetry of
the mucosal wave; and 6) glottic axis deviation.
Descriptive statistics (including median, interquartile
range [IQR], frequency, and percent) for demographic and
Fig. 3. Vascular lake on the lateral half of the superior surface of
the right vocal fold. Medial to it is a linear varix.
Tang et al.: Vocal Fold Varices and Hemorrhage
 TABLE I.
Summary of Studied Patients.
Total Patients Without Varix Patients With Varix P Value (Sig)

N 499 387 (77.6%) 112 (22.4%)

Male (%) 198 (39.7%) 159 (41%) 39 (34.8%) P 5 0.22
Female (%) 301 (60.3%) 228 (59%) 73 (65.2%) P 5 0.22
Median age–years (IQR)* 31.3 (17.2) 31.8 (18.2) 31.3 (16.1) P 5 0.398

*Wilcoxon two-sample test for difference in median age between varix groups.
IQR 5 interquartile range.

clinical variables of interest were calculated to characterize the
study cohort. The relationships between the presence/absence of
varices and 1) gender, 2) presence of mucosal lesions, and 3)
paresis were assessed by chi-square test, as were the relation-
ships between presence/absence of hemorrhage and these same
variables. The relationships between age and 1) presence/
absence of varix and 2) presence/absence of hemorrhage were
assessed by the Wilcoxon rank-sum test. In the group of
patients with varices, Fisher’s exact test was used to assess the
relationship between the various varix characteristics and the
incidence of hemorrhage. Kaplan-Meier survival analysis was
conducted to evaluate the failure (hemorrhage) probability and
to take into account the varying length of follow-up for patients
who came into the study at different times. Patients who did
not experience hemorrhage by the end of the follow-up period
were censored in the survival analysis. The log-rank test was
performed to determine whether time to hemorrhage differed
based on the presence or absence of varix. The median time to
hemorrhage and associated 95% confidence interval (CI), as
well as the hemorrhage proportion and associated 95% CI at
defined time points of interest, were estimated for both groups
(varix/no varix) when applicable. Cox proportional hazards
regression was used to estimate the univariate hazard ratio
(HR) (i.e., ratio of the rate of hemorrhage in the varix group
divided by the no varix group) and associated 95% CI. The pro-
portional hazards assumption was tested before carrying out
the Cox regression, and no evidence was found to indicate that
the HR was not constant over time in the study cohort. A multi-
variable model was not possible due to the low number of hem-
orrhage events. All P values are two-sided, with statistical
significance evaluated at the 0.05 alpha level. Ninety-five per-
cent CIs were calculated to assess the precision of the obtained
estimates. All analyses were performed in SAS 9.4 (SAS Insti-
tute Inc., Cary, NC) and Stata Version 13.0 (StataCorp, College
Station, TX).
cant difference in the median follow-up time between
the varix and nonvarix groups (P 5 0.87).
Incidence and Rate of Hemorrhage
The overall incidence of hemorrhage in the sample
was 1.08 cases per 1,000 person-months. The incidence
rate of hemorrhage was 3.3 cases per 1,000 person-
months in the varix group and 0.5 cases per 1,000
person-months in the nonvarix group. From the
Kaplan-Meier failure plot (Table II), we observed that
the varix group had a higher probability of hemorrhage
throughout the follow-up period compared to the non-
varix group (P 5 0.005, by log-rank test). The median
time to hemorrhage in the varix group was 40.1 months
(95% CI 5 34.8 months, upper limit not estimable). The
median time to hemorrhage and 95% CI were not esti-
mable in the nonvarix group. The hemorrhage probabil-
ity in the varix group was 2.7 % (95% CI 5 0.9%, 8.1%)
at 10 months, 5.3% (95% CI 5 2.2%, 12.6%) at 30
months, and 64.4% (95% CI 5 30.4%, 94.7 %) at 50
months. The hemorrhage probability in the nonvarix
group was 0.8% (95% CI 5 0.3%, 2.4%) at 10 months
TABLE II.
Hemorrhage Probability Over Time in Patients With and
Without Vocal Fold Varices.* [Color figure can be viewed in the
online issue, which is available at www.laryngoscope.com.]
HR 95% CI P Value
Varix (yes vs. no) 10.1 (3.2, 31.8) 0.0001

RESULTS
Study Population
Five hundred and thirteen performers presented for
care during the period of review. Fourteen presenting
with hemorrhage at their initial visit were excluded.
The demographic information of the remaining 499
patients is presented in Table I. Patients with varix did
not differ significantly from those without varix in gen-
der or age (P 5 0.22 and P 5 0.40, respectively).
Patients with hemorrhage did not differ significantly
from those without in age (P 5 0.41). A minimum of 12
months elapsed after the index visit for all patients; the
median overall follow-up time was 24.8 months in the *Cox proportional hazards regression.
cohort (IQR 5 13.1). There was no statistically signifi- CI 5 confidence interval; HR 5 hazard ratio.

Laryngoscope 126: May 2016 Tang et al.: Vocal Fold Varices and Hemorrhage
1165
 TABLE III. 44 cases, of which only one had to be addressed surgi-
Varix Characteristics and Hemorrhage. cally—presumably for recurrent hemorrhage.10 The bal-
ance of the literature3,5–7 consists of surgical series
Hemorrhage No Hemorrhage
focused on technique, particularly the use of angiolytic
Frequency (%) P Value*
lasers, leaving the question of when to operate largely
unaddressed. Among these, recurrent hemorrhage
Pinpoint 5 (8.77) 52 (91.23) 1.000 remains a prominent indication for intervention, but
No pinpoint 4 (7.27) 51 (92.73) authors also cite resection during surgery for other
Linear 3 (5.88) 48 (94.12) 0.5063 lesions, even in the absence of hemorrhage3,6,7; one
No linear 6 (9.84) 55 (90.16) group speaks of preemptive surgery of varix alone.5
Lake 2 (9.09) 20 (90.91) 1.000 Our patient population, limited to performers, dem-
onstrated a markedly higher prevalence of varices than
No lake 7 (7.78) 83 (92.22)
the only extant general patient series (22.4% vs. 3.1%).8
Right edge 1 (5.26) 18 (94.74) 1.000
The discrepancy is less stark when only professional
No right edge 8 (8.360) 85 (91.40)
voice patients are considered (22.4% vs. 9.5%). The com-
Left edge 2 (8.33) 22 (91.67) 1.000 parison article includes vocally intensive professions
No left edge 7 (8.05) 80 (91.95) such as schoolteachers in the professional voice category;
*Fisher’s exact test
the stricter definition used in our series may account for
some of the residual disparity. Advances in optics over
17 years since the comparison article was written, par-
and 30 months, 4.9% (95% CI 5 1%, 23.4%) at 50
ticularly distal-chip endoscopy and high definition cam-
months, and 12.2% (95% CI 5 3.3%, 40.0%) at 80 eras, may account for more.
months. Many authors point to female preponderance as evi-
The Cox proportional hazard regression model dence of a hormonal role in varix formation. Although
found that patients with varix (compared to patients hormonal effects generally loom large in both popular
without varix) had a HR of 10.1 (95% CI 5 3.2%, 31.8%). and professional explanations of voice change in women,
Specifically, the varix group had 10 times the rate of particularly in performers, studies are few and of gener-
hemorrhage compared to the nonvarix group over the ally low quality; no clear evidence of causation exists.
follow-up period in this study (P < 0.0001). Apparently overlooked is the general preponderance of
women among patients with voice complaints, probably
Varix Characteristics because intrinsic differences in anatomy and phonatory
The Fisher’s exact test did not provide any evidence physiology predispose to phonotraumatic injury. The pro-
of association between varix type or location and inci- portion of women in our series (65.2%) as well that of
dence of hemorrhage (Table III). Postma et al. (53.3%)8 is not markedly different from

TABLE IV.
Other Vocal Fold Pathology Gender and Associated Pathology.
Overall, 274 (55%) of patients had mucosal lesions,
Hemorrhage No Hemorrhage
117 patients (23%) were diagnosed with paresis. There
was no statistically significant difference in the propor- Variable Frequency (%) P Value*
tion of patients with varix or in the proportion of
patients experiencing hemorrhage between 1) patients Female 11 (3.61) 294 (96.39) 0.2661
with or without mucosal lesions or 2) patients with or Male 3 (1.55) 191 (98.45)
without paresis (Table IV). Mucosal lesion 8 (3.27) 237 (96.73) 0.5963
No mucosal lesion 6 (2.36) 248 (97.64)
DISCUSSION Paresis 3 (2.56) 114 (97.44) 1.000
Although a relationship between vocal fold varices No paresis 11 (2.88) 371 (97.12)
and hemorrhage seems intuitive and has been long *Pearson’s chi-square test.
assumed, it has never been precisely defined. Baker
appears to have offered the initial description of surgical Varix No Varix

management of vocal fold varices.9 In this report of

Variable Frequency (%) P Value
three cases, Baker characterized varices as a problem of
vocal performers and established recurrent hemorrhage Female 74 (24.26) 231 (75.74) 0.2224
as the dominant indication for removal. Systematic Male 38 (80.41) 156 (19.59)
study was not undertaken until 1998, when Postma Mucosal lesion 61 (24.90) 184 (75.10) 0.1971
et al. reported an incidence of varix in 25 of 800 (3.1%) No mucosal lesion 51 (20.08) 203 (79.92)
of patients presenting to a voice center, of which 13 Paresis 26 (22.22) 91 (77.78) 0.9474
(52%) were performers.8 Two were subsequently oper-
No paresis 86 (22.51) 296 (77.49)
ated for recurrent hemorrhage. In a study of hemor-
rhage, Lin et al. found an incidence of varices in nine of *Pearson’s chi-square test

Laryngoscope 126: May 2016 Tang et al.: Vocal Fold Varices and Hemorrhage
1166
that in a series of patients from our center with all
benign lesions (62.8%)11 or in a series of performers with
voice complaints (54%).12 The proportion of women in
surgical series of varix is generally consistent: 53%3,
57%5, and 58%7, although it is 81% in Hochman et al.6
Examination of the Kaplan-Meier failure curves
and assessment of hemorrhage probabilities at selected
time points indicate that the varix group had a higher
probability of hemorrhage throughout the follow-up
period compared to the nonvarix group. The HR of 10.1
(95% CI 5 3.2, 31.8) suggests that the varix group had
10 times the expected hazard or risk of hemorrhage com-
pared to the nonvarix group. At the same time, it is
equally important to note that the overall incidence of
hemorrhage is low, even in the varix group. There are
no directly comparable data in the extant literature.
Hemorrhage is presumed to occur when mechanical
stress from mucosal displacement results in the shearing
of vessel walls. Hochman et al. proposed that this trauma
was greatest at the lateral edge of the membranous vocal
fold where “the mucosal wave . . . decelerates quickly, and
reverses direction to begin the closing phase of the oscilla-
tory cycle.”6 Alternately, one might expect traumatic
forces to be greatest at the vibratory margin, where the
mucosal displacement is greatest and perhaps augmented
by collision trauma. Analysis based on location of the
vocal fold varix revealed no difference in hemorrhage rate
based on the location of the varix on the vocal fold. Simi-
larly, one may speculate that the more dysmorphic the
varix, the likelier it is to tear; the morphology of the varix
did not influence rate of hemorrhage.
We hypothesized that the presence of mucosal
lesions and/or paresis may increase the risk of hemor-
rhage by decreasing phonatory efficiency and increasing
phonotraumatic stress. Additionally, the presence of
mucosal lesions, most of them phonotraumatic, may
serve as a proxy indicator for phonotrauma. Although
significantly more patients with mucosal lesions had
varices, neither of these two clinical findings appeared
to influence the rate of hemorrhage in this sample.
This study had several limitations. This study used
the first evaluation of varix for repeat patients assessed
during the August 2012 to July 2014 study period,
resulting in accrual of longer follow-up times for repeat
patients. Repeat patients may be likely to have more sig-
nificant voice-related complications compared to patients
with a single visit. Not every patient was reassessed at
a given interval to verify status, but only if he or she
presented for care. Among performers, we do not believe
that a significant number of hemorrhages would have
been overlooked by dint of patients not presenting for
evaluation, but it is certainly possible that patients
sought care elsewhere.
Generalizing the findings of this study to a broader
population must be circumspect. Performers are a subset
of patients subject to higher than normal phonotrau-
matic stress, as demonstrated by a markedly higher inci-
dence of phonotraumatic lesions in comparison to
nonperformers.12 In addition, they are likely more aware
of voice change and quicker to seek evaluation for it.
Thus, hemorrhage in this group may both occur at a
Laryngoscope 126: May 2016
TABLE V.
Overview of Hemorrhage Rates.
Patients With Patients Without
Varices Varices
Rate of hemorrhage at 10 months 2.7% 0.8%
Rate of hemorrhage at 30 months 5.3% 0.8%
Rate of recurrent hemorrhage13 47.8% 4.17%
higher rate and be more likely to come to medical atten-
tion than in the general population. Performers are typi-
cally a younger group than the patients from the
general population and therefore may be expected to be
healthier and less likely to be on anticoagulant medica-
tion. On the other hand, contraceptives use is likely
higher among younger women, potentially affecting hor-
monal factors to which previous authors allude.
Finally, the impact of hemorrhage may not be fully
represented by incidence or relative risk alone. Each inci-
dent of hemorrhage imposes a period of professional
absence (for performers at least) necessary for recovery.
However, the most frequently stated fear in patients who
have hemorrhaged concerns the long-term risk of vocal
fold scar and its consequences. This remains undefined.
As in the case of varices, the long-term risks of hemor-
rhage represent another area in which data is absent.
Available data regarding varices and hemorrhage is
summarized in Table V. Although patients with varix have
an appreciably higher risk of hemorrhage and the risk of
surgery appears to be low,3,5–7 so too does the incidence of
hemorrhage. Lennon et al. have examined the risk of
recurrence in patients with hemorrhage.13 In that group,
not limited to performers, patients with varices had a 48%
chance of recurrent hemorrhage, twelvefold greater than
patients without varix. Based on these results, we do not
recommend surgery for otherwise asymptomatic varices in
patients with no history of hemorrhage, regardless of varix
morphology or location on the vocal fold. We do recom-
mend that varices in patients with one or more incidences
of vocal fold hemorrhage be addressed, particularly in per-
formers. Techniques include angiolytic laser ablation, as
described elsewhere,3,5,7 which is favored for varices on
the superior surface of the vocal fold, and cold-knife surgi-
cal excision for vibratory margin lesions if there is concern
that a small mass lesion may remain after laser ablation,
even when the vessel is obliterated.
CONCLUSION
Vocal fold varices were found in approximately one-
fifth of vocal performers presenting for evaluation,
regardless of gender. The overall incidence of hemor-
rhage in the sample was 1.08 cases per 1,000 person-
months. The incidence rate of hemorrhage was 3.3 cases
per 1,000 person-months in the varix group and 0.5
cases per 1,000 person-months in the nonvarix group.
Neither the location of the varix or its morphology
appears to influence the risk of hemorrhage, nor does
the presence of other pathology. Although the rate of
hemorrhage is significantly higher in patients with
Tang et al.: Vocal Fold Varices and Hemorrhage
1167
varix, the overall incidence is low. Surgeons should take
this data into account in treating vocal fold varices in
patients without a history of hemorrhage.
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