Am J Otolaryngol xxx (xxxx) xxxx

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Am J Otolaryngol
journal homepage: www.elsevier.com/locate/amjoto

Classification of laryngeal injury in patients with prolonged intubation and

to determine the factors that cause the injury
Dursun Mehmet Mehel , Doğukan Özdemir, Mehmet Çelebi, Samet Aydemir, Gökhan Akgül,
⁎

Abdulkadir Özgür
University of Health Sciences-Samsun Health Practices and Research Center, Department of Otorhinolaryngology, Samsun, Turkey

ARTICLE INFO ABSTRACT

Keywords: Objective: This study aims to evaluate injuries occurring in the larynx of patients intubated in intensive care units
Larynx for a long time.
Laryngeal injury Study design: Prospective clinical study.
Prolonged entubation Setting: Tertiary hospital.
Entubation time
Subject and methods: Between April 15, 2019, and November 15, 2019, 40 patients who were hospitalized in
Tracheotomy
Classification
intensive care units had a tracheotomy procedure due to prolonged intubation, and laryngeal structures were
evaluated by direct laryngoscopy. The laryngeal structures were evaluated in four groups as glottic-supraglottic
region, arytenoid vocal process, interaritenoid region and subglottic region. Edema, granulation and ulceration
findings in these four regions were recorded. The injuries to the laryngeal structures were classified as stages
0–3. As a result of the data obtained, the relationship between the degree of laryngeal lesions and the factors that
may cause these lesions was investigated.
Results: According to our classification, nine patients had stage 1, 16 patients had stage 2 and 15 patients had
stage 3 laryngeal injury. There was no significant relationship between the stage of laryngeal injury and age, sex
and diameter of the intubation tube. There was a statistically significant relationship between laryngeal injury
and the day the tracheotomy was performed (p = 0.007).
Conclusion: In patients that had prolonged endotracheal intubation, injury to the laryngeal structures is in-
evitable. To minimize this occurrence, tracheotomy should be performed for intubations that extend for more
than seven days. When performing the tracheotomy, the laryngeal structures should be evaluated, necessary
precautions should be taken for the traumatic lesions that are difficult to heal, and treatment should be started.

1. Introduction
Endotracheal intubation is a widely used method for providing
short-term safe airway. Laryngeal complications are not uncommon in
prolonged endotracheal intubation, and treatment is long and tedious
for both the patient and the physician. While tracheotomy is used for
long-term airway access in ventilator-dependent patients, there is no
consensus on an ideal time to perform a tracheotomy. However, pro-
spective studies have shown that endotracheal intubation longer than
seven days increases the likelihood of serious injury to laryngeal
structures [1–5].
Changes in the laryngeal mucosa due to endotracheal intubation are
inevitable. Laryngeal injury begins within the first few hours and con-
tinues with each day of intubation [6]. The important point in mucosal
injury is capillary perfusion. When the pressure in the wall of the en-
dotracheal tube exceeds the mucosal capillary pressure, first irritation
occurs, then congestion, edema and ultimately ulceration along with
ischemia. Progressive ulceration causes perichondritis, chondritis, and
finally necrosis, including cricoarytenoid joints and cricoid cartilage
[7,8]. The degree of injury depends on several factors, including the
duration of intubation, the size of the tube, the general condition of the
patient, and the presence of infection. It is important to diagnose these
changes as soon as possible to prevent irreversible sequelae of intuba-
tion [9,10].
Tracheotomy procedures in patients with prolonged endotracheal
intubation lead to a reduction in injury to the laryngeal structures,
ensuring a safe airway, aspiration of respiratory secretions, a switch to
oral feeding, communication with the patient, early discharge from

⁎
Corresponding author at: University of Health Sciences-Samsun Health Practices and Research Center, Department of Otorhinolaryngology, Kadıköy Mah. Park
Sok. No: 199, PB: 55090, İlkadım, Samsun, Turkey.
E-mail address: doktormehel@gmail.com (D.M. Mehel).

https://doi.org/10.1016/j.amjoto.2020.102432
Received 15 January 2020
0196-0709/ © 2020 Published by Elsevier Inc.

Please cite this article as: Dursun Mehmet Mehel, et al., Am J Otolaryngol, https://doi.org/10.1016/j.amjoto.2020.102432
D.M. Mehel, et al. Am J Otolaryngol xxx (xxxx) xxxx

intensive care unit, and increased mobilization and comfort of the pa-
tient [5,11–13].
This study aimed to evaluate the laryngeal injury in the 40 patients

Ulceration unilaterally or bilaterally at cricoarytenoid region,

Deep ulceration, partial necrosis and widespread granulation
that were hospitalized in intensive care unit and intubated for a long
time during a tracheotomy procedure by direct laryngoscopy to give the
findings obtained a new classification and determine the factors causing

Ulceration/circumferential leaf shaped granulation

the injury.

2. Materials and methods

Stenosis by circumferential granulation

sometimes with exposed cartilage.
This prospective study was approved by the Ethics Committee of the
University of Health Sciences Samsun Education and Research Hospital
(Decision No: TUEK 37-2019BADK/8-63). Informed consent was ob-
tained from the first-degree relatives of the patients included in the
study.
The study was planned prospectively. Forty patients who were
hospitalized in intensive care units between April 15, 2019, and

Grade 3
November 15, 2019, in our hospital and underwent tracheotomy due to

Severe
prolonged intubation were included in the study. Each patient was seen
by an otolaryngologist in the intensive care unit before the tracheotomy

Prominent granulation at posterior part extended laterally

procedure. Patients who had a tracheotomy under 18 years of age,
congenital or acquired laryngeal disease, history of trauma or radio-

Ulceration/anteriorly located moderate granulation

Ulceration and granulation at the ulceration edges

therapy to the neck, antiaggregant treatment or hematologic disease
were not included in the study. Preoperative blood count, biochemistry,
prothrombin time and partial thromboplastin time were evaluated.
The patients underwent a tracheotomy under general anesthesia
with an appropriate surgical method. After confirming that the cannula
was in the tracheal lumen and the patient's lungs was ventilated, the

and ulceration area in pieces

cannula was fixed and the laryngoscopy procedure was started. Direct

extended glottis bilaterally

laryngoscopy was performed by an otolaryngologist who did not know
the patient's history. The laryngeal structures and subglottic region up
to the tracheotomy cannula were evaluated by laryngoscopy using
microscopes and telescopes (0° and 30°). The laryngeal structures were
evaluated in four groups as glottic-supraglottic region, arytenoid vocal
Moderate
Grade 2

process, interarytenoid region and subglottic region. Edema, granula-

tion and ulceration findings in these four regions were recorded. No
intervention was made to the observed pathological tissues. Two clin-
Mild ulceration/tongue shaped mild granulation extended to

icians then classified the laryngeal lesions according to the classifica-

tion criteria summarized in Table 1, taking into account the information
in the form.
Staging of the injury to the larynx and subglottic region due to prolonged intubation.

In addition to the laryngeal pathological findings of the patients

included in the study, age, sex, primary disease, day of intubation on
which tracheotomy was performed, the diameter of the intubation tube
Hyperemia and edema at posterior part

used, and early–late complications due to tracheotomy were recorded.

Prominent entubation tube groove

As a result of the data obtained, the relationship between the level of

glottis unilaterally or bilaterally

laryngeal lesions and the factors that may cause these lesions was in-
vestigated.
The data were analyzed with SPSS version 15.0 for Windows (SPSS
Inc., Chicago, IL, USA). The results were presented as means ±
standard error of measurement. All data were analyzed with a one-way
analysis of variance (ANOVA) post hoc Bonferroni test. A p-value
of < 0.05 was considered to indicate a significant difference.
Grade 1

Mild

3. Results
Grade 0

Normal
Normal

Normal
Normal

Of the 40 patients included in the study, 27 were male and 13 were

female, with a mean age of 69.6 ± 16.5 years, ranging from 24 to
100 years. Primary conditions were neurological diseases in 20 cases,
Glotticand supraglottic edema

multi-organ failure in 11 cases, respiratory diseases in five cases, and

oncological diseases in four cases.
Arytenoidvocal process

Interarytenoid region

According to our classification, 9 patients had Grade 1, 16 had

Subglottic region

Grade 2 and 15 had Grade 3 laryngeal injuries (Figs. 1, 2 and 3).

Larynx injury

There was no significant relationship between the stage of the lar-

yngeal injury and the age and sex of the patients. There was no sig-
Table 1

nificant relationship between the diameter of the intubation tube and

the degree of laryngeal injury. There was a statistically significant

2
D.M. Mehel, et al. Am J Otolaryngol xxx (xxxx) xxxx

Fig. 1. Grade 1 laryngeal and subglottic injury. A) Edema in the vocal cords. B) Tongue shaped mild granulation in the vocal processes of the arytenoid. C) Prominent
endotracheal tube groove and mild ulceration in the posteriorglottic region. D) Granulation tissue originating from the posterior in the subglottic region and
protruding into the lumen.

relationship between laryngeal injury and the day tracheotomy was care unit. In our study, a surgical tracheotomy was performed seven to
performed (p = 0.007). The data obtained are summarized in Table 2. 28 days on average, 16 days after intubation in all patients with
Two of the patients who underwent surgical tracheotomy had sub- transoral endotracheal intubation due to 20 neurological, 11 multi-
cutaneous emphysema in the head and neck region, and three patients organ failure, five respiratory disease and four oncologic causes, all
had bleeding around the tracheotomy cannula that required no inter- hospitalized in intensive care units. The diameter of the endolaryngeal
vention. There was no late complication during the follow-up period. tubes used in the patients ranged from 6 mm to 8.5 mm.
Some authors classify laryngeal and tracheal injury differently due
to prolonged endotracheal intubation over the years. Lindholm [21] did
4. Discussion
his classification according to the extent and depth of mucosal injury
caused by prolonged intubation of the larynx and trachea. Santos et al.
Advances in medical treatment have led to an increase in patients
[4] evaluated patients with prolonged intubation according to findings
requiring airway support in intensive care units. Despite technological
of laryngeal injuries. They identified risk factors for laryngeal injury in
advances in the biocompatibility of materials used in endolaryngeal
97 patients intubated for more than three days (mean nine days). They
tubes and efforts to reduce trauma due to prolonged intubation, lar-
found laryngeal erythema in 94%, ulceration in 76%, and laryngeal
yngeal and tracheal lesions remain a problem. Nowadays, a tra-
granuloma in 44% (57% of granulomas occurred on average four weeks
cheotomy is opened to increase the comfort of patients hospitalized in
after extubation). Colton et al. [22] classified the injury in laryngeal
intensive care units rather than providing emergency airway by redu-
structures due to prolonged intubation as mild, moderate and severe.
cing the complications related to endotracheal intubation and me-
Benjamin classified laryngeal injury after prolonged intubation into five
chanical ventilator [14]. Goldenberg et al. [15] found that the need for
stages as early and nonspecific changes, edema, ulceration, granulation
a tracheotomy was most frequent in intensive care units (32%) in 1130
tissue and multiple injuries (arytenoid dislocation, vocal cord lacera-
patients. The ages of the patients included in this study ranged from 24
tion, intrinsic muscle injury, airway perforation, and mediastinal em-
to 100 years, with an average age of 69.6 years, and all 40 patients
physema) [9]. In our study, we classified the laryngeal and subglottic
included in the study were admitted to intensive care units.
injury caused by prolonged endotracheal intubation into four stages
Prolonged transoral endotracheal intubation increases orophar-
according to anatomic location and depth of mucosal injury.
yngeal contamination of the lungs, increasing the risk of ventilator-
Colton et al. evaluated laryngeal structures with a flexible endo-
associated pneumonia, and may also cause sinusitis and severe lar-
scope in 61 patients aged 19 to 80 years after an intubation period of
yngeal and tracheal injuries. Tracheotomy has become a viable alter-
two to 28 days. They found no correlation between age, height, sex,
native to long-term endotracheal intubation in patients with prolonged
weight and laryngeal injury. Also, there was no statistically significant
intubation, with the advantages of increasing patient comfort, reducing
relationship between laryngeal injury, intubation time and intubation
sedation, reducing airway resistance and allowing easier airway
tube size. However, they found that, when laryngeal injury increased,
maintenance [16–18]. Many authors recommend making tracheotomy
vocal cord movements decreased, and ulceration and granulation tissue
available to patients with chronic respiratory failure after a 7–9-day
were formed in posterior glottis with increasing intubation time [22].
intubation to prevent long-term injury to the larynx and trachea
Santos et al. reported that long-term intubation-related pathologies
[19,20]. In a survey of 429 physicians from 59 countries [20], Vargas
were significantly associated with intubation time and the presence of a
et al. found that tracheotomies were most frequently performed
nasogastric tube [4]. In our study, no statistically significant
(54.4%) between seven and 15 days after admission to the intensive

Fig. 2. Grade 2 laryngeal and subglottic injury. A) Ulceration at vocal process of arytenoid, adherent tongue shaped granulation tissue in the anterior region. B) Leaf
shaped granulation that holds interarytenoid region and vocal process of arytenoid. C) Ulceration and granulation atinterarytenoid region and cricoarytenoid joint
region.

3
D.M. Mehel, et al. Am J Otolaryngol xxx (xxxx) xxxx

Fig. 3. Grade 3 laryngeal and subglottic injury. A) Circumferential granulation glottic level and synechia in anterior part of vocal cords. B) Deep ulceration at
interarytenoid and cricoarytenoid region. C) Circumferential ulcerated granulation tissue that filling the lumen almost completely.

Table 2
The relationship between grade of laryngeal injury and age, sex, endotracheal tube diameter and tracheotomy performing day.
Grade 0 (n = 0) Grade 1 (n = 9) Grade 2 (n = 16) Grade 3 (n = 15) p⁎

Agea – 67.3 ± 17.3 (43–86) 66.3 ± 17.2 (24–92) 74.4 ± 15.2 (43–100) p = 0.364
Gender M/F – 8/1 10/6 8/7 p = 0.214
Endotracheal tube diameter – 7.5 (n = 3) 7 (n = 1) 6 (n = 1) p = 0.418
8 (n = 6) 7.5 (n = 10) 7 (n = 2)
8 (n = 3) 7.5 (n = 7)
8.5 (n = 2) 8 (n = 3)
8.5 (n = 2)
Tracheotomy performing daya – 12.1 ± 3.1 (10−20) 16.8 ± 5.3 (7–25) 19.5 ± 5.9 (12–28) p = 0.007

⁎
p < 0.05 statistically significant.
a
Values are as follows mean ± SD (min-max).

relationship was found between the grade of the laryngeal and sub-
glottic injury due to prolonged intubation and age, sex, and diameter of
the intubation tube used. However, a statistically significant correlation
was found between the grade of injury and the day of the tracheotomy
procedure.
Astrachan et al. evaluated 52 patients who underwent a tra-
cheotomy after prolonged endotracheal intubation and found the
complication rate due to endotracheal intubation to be 57% and the
complication rate due to a tracheotomy to be 14%. They also reported
tracheotomy complications as non-serious. They concluded that tra-
cheotomy provides practical and psychological benefits and can be
performed safely in patients with prolonged intubation [23]. In our
study, direct laryngoscopy performed after prolonged intubation re-
vealed laryngeal and subglottic injury at different stages in all 40 pa-
tients. Tracheotomies revealed non-significant stomal bleeding in three
patients and subcutaneous emphysema in two patients. There was no
problem during long-term follow-ups.
Our study provides important data demonstrating laryngeal damage
caused by long-term intubation. It also proposes a new classification to
show the resulting laryngeal injury. However, the complications caused
by laryngeal damage in the long term cannot be detected, and the
sample size of the study group is limited, limiting the effectiveness of
the study.
5. Conclusion
In patients who had prolonged intubation, injury to the laryngeal
structures is inevitable. Tracheotomy should be performed for intuba-
tions that extend for more than seven days to minimize this occurrence.
When performing a tracheotomy, the laryngeal structures should be
evaluated and the necessary precautions taken for the traumatic lesions
that are difficult to heal, and treatment should be started afterward. We
believe that prospective studies and long-term follow-ups are needed
for the classification of laryngeal injury due to prolonged intubation.
Author statement
Dursun Mehmet Mehel: Conceptualization, methodology, data
curation, writing.
Doğukan Özdemir: Data curation, investigation.
Mehmet Çelebi: Methodology, data curation, investigation.
Samet Aydemir: Data curation, investigation, writing.
Gökhan Akgül: Data curation, investigation.
Abdulkadir Özgür: Conceptualization, methodology, writing- re-
viewing and editing.
Ethical approval
This study was approved by the Ethics Committee of the University
of Health Sciences Samsun Education and Research Hospital (Decision
No: TUEK 37-2019BADK/8-63).
Funding
The author(s) received no financial support for the research.
Informed consent
Written informed consent was obtained from patients or their re-
latives.
Declaration of competing interest
The authors declare no conflict of interest.
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