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ORIGINAL ARTICLE

Factors Associated With Hypertrophy


of the Lingual Tonsils in Adults
With Sleep-Disordered Breathing
Myung-Whun Sung, MD; Woo Hyun Lee, MD; Jee Hye Wee, MD;
Chul Hee Lee, MD; Eunhee Kim, MD; Jeong-Whun Kim, MD, PhD

Importance: This study shows factors affecting lingual Results: A total of 97 subjects were included in this study.
tonsil hypertrophy (LTH) in sleep-disordered breathing. The median (interquartile range) apnea hypopnea in-
dex was 16.5/h (7.6/h-27.5/h). The median (interquar-
Objective: To identify the factors associated with LTH tile range) thickness of the lingual tonsils as measured
in adults with sleep-disordered breathing. by MRI was 3.6 mm (1.9-5.2 mm) and 4.9 mm (2.9-6.7
mm) in the midline and paramidline of the tongue base,
Design: Retrospective analysis. respectively (P ⬍ .001). Laryngopharyngeal reflux (re-
flux finding score ⬎7) was present in 32 patients. The
Setting: Academic tertiary referral center.
endoscopic grade of LTH agreed with the radiographic
grade (␬ = 0.731; P ⬍ .001). Lingual tonsil thickness as
Participants: Ninety-seven adult patients with obstruc-
measured by MRI was correlated with the endoscopic
tive sleep apnea, who visited the Department of Otorhi-
nolaryngology sleep clinic, were included from Febru- grade of LTH (P⬍ .001). Multivariate analysis revealed
ary 2009 through August 2011. that laryngopharyngeal reflux (P ⬍.001) and body mass
index (P =.046) were independently significant factors
Interventions: All patients underwent WatchPAT (pe- associated with LTH as measured by MRI.
ripheral arterial tone) examination, endoscopic exami-
nation of the upper airway, simple skull lateral radiog- Conclusions and Relevance: Reflux finding score and
raphy, and cine magnetic resonance imaging (MRI) sleep body mass index were significantly associated with LTH
study of the upper airway tract. in adults with sleep-disordered breathing, whereas the
respiratory parameters were not associated with LTH.
Main Outcomes and Measures: Prognostic factors
indicating LTH in adults with sleep-disordered breathing. JAMA Otolaryngol Head Neck Surg. 2013;139(6):598-603

T
HE LINGUAL TONSILS CON- such as phenytoin.9 The evaluation of LTH
stitute the Waldeyer ring can be performed by endoscopic exami-
along with the palatine ton- nation, magnetic resonance imaging
sils, adenoids, tubal ton- (MRI), computed tomography, or simple
sils, and lateral pharyn- skull lateral radiography. There have been
geal bands.1 Hypertrophy of the lingual a few studies performing systematic analy-
tonsils has several clinical implications ses of multiple factors that might be asso-
such as dysphagia, upper airway obstruc- ciated with LTH in adults. This study was
tion, difficult intubation, and difficult gas- aimed to identify the factors associated
trointestinal endoscopy because the lin- with LTH in adults with sleep-disordered
Author Affiliations: gual tonsils are located in the tongue breathing. Author Aff
Department of Departmen
Otorhinolaryngology, Seoul base.2-5 In particular, lingual tonsil hyper- Otorhinola
National University College of trophy (LTH) has been thought to be an METHODS National Un
Medicine, Seoul, South Korea important factor for the development of Medicine, S
(Drs Sung, W. H. Lee, Wee, sleep-disordered breathing including (Drs Sung,
C. H. Lee, and J.-W. Kim); and SUBJECTS C. H. Lee, a
simple snoring and obstructive sleep ap-
Department of Radiology nea (OSA). Several causes might be con- Departmen
(Dr E. Kim), Seoul National Subjects who underwent sleep apnea screen- (Dr E. Kim
University Bundang Hospital,
tributing to LTH such as reactive lym- ing examinations at Gangnam Healthcare Cen- University
Seongnam, South Korea phoid hyperplasia due to previous ter of Seoul National University Hospital from Seongnam,
(Drs W. H. Lee, Wee, and adenotonsillectomy,6 laryngopharyngeal February 2009 through August 2011 were in- (Drs W. H.
J.-W. Kim). reflux,7 obesity,8 and use of medications cluded in this study. All the subjects com- J.-W. Kim).

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A B C

D E F

Figure 1. Grading of lingual tonsil hypertrophy. Endoscopically, grade 1 (A), grade 2 (B), and grade 3 (C). Radiographically, grade 1 (D), grade 2 (E), and grade 3 (F).

plained of habitual snoring or sleep apnea. The exclusion crite- lecula by a blinded radiologist using the simple skull lateral ra-
ria were as follows: younger than 19 years, the presence of cardiac diograph: grade 1, minimal irregularity of the tongue base by
arrhythmia, use of ␣-adrenergic receptor blockers (a washout the lingual tonsil opacity with the vallecula fully visible; grade
period of ⬎24 hours was required), history of bilateral cervical 2, lingual tonsil opacity with the vallecula partially obscured;
or thoracic sympathectomy, and peripheral vasculopathy or neu- grade 3, lingual tonsil opacity with the vallecula totally ob-
ropathy. This study was approved by the institutional review board scured; and grade 4, lingual tonsil opacity extending over the
of Seoul National University Bundang Hospital. epiglottis (Figure 1).
All patients underwent a cine MRI sleep study of the upper
STUDY PROTOCOL airway as described elsewhere.10 For a dynamic airway exami-
nation, presedation and postsedation MRI images were ob-
The sleep apnea screening examinations included WatchPAT (pe- tained, but only presedation axial views were used in the pres-
ripheral arterial tone) (Itamar Medical Ltd) performed at home ent study. Subjects were placed in the supine position with
and endoscopic examination of the upper airway tract (includ- their head and neck fixed in the neutral position. They were
ing the nasal cavity, oral cavity, oropharynx, larynx, and hypo- instructed to breathe in and out naturally. The MRI images
pharynx), simple skull lateral radiography, and a cine MRI sleep were evaluated by a sleep specialist ( J.-W.K.) and a radiolo-
study of the upper airway tract (Intera Achieva 1.5T; Philips Medi- gist (E.K.), who were blinded to the results of WatchPAT test-
cal Systems) performed at the Gangnam center. The parameters ing, endoscopy, and simple radiography. The lingual tonsils
obtained from the WatchPAT device concerned respiratory events, showed high signal intensity at the posterior aspect of the
sleep position, oxygen desaturation, and snoring. tongue base in the T2-weighted imaging. The thickness of the
lingual tonsils including tongue base mucosa was measured in
EVALUATION OF LTH the anterior-posterior dimension, where the high signal inten-
sity was greatest in the whole tongue base. The thickness of
The lingual tonsils were endoscopically graded on scale from the tongue base mucosa per se was also measured (Figure 2).
0 to 4 based on their distribution and visibility of the vallecula The net thickness of the lingual tonsils was obtained by sub-
and epiglottis by a blinded examiner using the endoscopic pho- tracting mucosal thickness in the midline and paramidline of
tographs taken with the tongue protruded: grade 0, no tonsils; the tongue base.
grade 1, spotted tonsil tissues with the tongue base vascula-
ture visible; grade 2, diffuse tonsil tissues with the tongue base EVALUATION OF
vasculature invisible; grade 3, diffuse tonsil tissues with the val- LARYNGOPHARYNGEAL REFLUX
lecula invisible; and grade 4, diffuse tonsil tissues with the epi-
glottis invisible (Figure 1). All patients underwent endoscopic laryngeal examination. The
The lingual tonsils were also radiographically graded on a endoscopic findings were evaluated based on the reflux find-
scale from 1 to 4 based on their size and visibility of the val- ing score system, which consists of 8-item endoscopic find-

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A B

Figure 2. Magnetic resonance imaging. Magnetic resonance images in 2 patients with prominent lingual tonsils (A) and scanty lingual tonsils (B). The lingual
tonsils were measured at 2 levels: at the uvula level (dotted line) and at the epiglottis level (solid line).

ings.11 A patient with a reflux finding score greater than 7 was two subjects had laryngopharyngeal reflux (reflux find-
diagnosed as having laryngopharyngeal reflux. ing score ⬎7). All patients were divided into 4 groups
according to the severity of sleep-disordered breathing:
STATISTICAL ANALYSIS 12 simple snorers (AHI ⬍5/h), 30 patients with mild OSA
(AHI ⱖ5/h to ⬍15/h), 35 with moderate OSA (AHI ⱖ15/h
All parameters were evaluated for normality using a Kolmogorov- to ⬍30/h), and 20 with severe OSA (AHI ⱖ30/h). The
Smirnov test. When the normality is unmet, the data are pre-
demographic, respiratory, and radiologic characteris-
sented as median (interquartile range [IQR]). Comparisons
among the 4 groups were performed using a Kruskal-Wallis test tics are given in Table 1. The presence of laryngopha-
for continuous variables and a ␹2 test for discrete variables. A ryngeal reflux was not significantly different among the
nonparametric paired test was performed using a Wilcoxon 4 OSA severity groups (P =.10).
signed rank test. Multiple stepwise regression analyses were per-
formed to determine any significant predictors among demo- THICKNESS OF THE LINGUAL TONSILS
graphic, respiratory, endoscopic, and radiologic parameters as-
sociated with LTH. Statistical analyses were performed using The median (IQR) thickness of the lingual tonsils as mea-
SPSS 18.0 software (SPSS Inc). P⬍.05 was considered statis-
sured by MRI was 3.6 mm (1.9-5.2 mm) and 4.9 mm (2.9-
tically significant.
6.7 mm) in the midline and paramidline of the tongue
base, respectively (P ⬍ .001). The mean of midline and
RESULTS paramidline lingual tonsil thickness was not signifi-
cantly different among the 4 OSA severity groups (P = .74)
CHARACTERISTICS OF STUDY SAMPLES (Table 1).
Endoscopically, 36 subjects had grade 1 LTH; 40, grade
A total of 97 subjects (13 women) were included in this 2; and 21, grade 3. The radiographic examination of skull
study. Their median age was 52 years (IQR, 47-57 years); lateral view showed that 43 subjects had grade 1 LTH;
body mass index (calculated as weight in kilograms di- 31, grade 2; and 23, grade 3. The endoscopic grade of
vided by height in meters squared) 25.8 (IQR, 23.9- LTH agreed with the radiographic grade (Cohen ␬ coef-
26.8); apnea hypopnea index (AHI), 16.5/h (IQR, 7.6/ ficient = 0.731; P ⬍ .001) (Table 2).
h-27.5/h); supine AHI, 26.4/h (IQR, 12.5/h-45.0/h); The mean of the midline and paramidline lingual ton-
oxygen desaturation index, 11.1 (3.6-20.2); minimal oxy- sil thickness measured by MRI was 2.5 mm (1.6-3.0 mm),
gen saturation, 85% (81%-88%); loudness of snoring, 46 4.9 mm (3.0-5.5 mm), and 8.1 mm (6.5-9.1) in endo-
dB (IQR, 44-50 dB); and the percentage of sleep time with scopic grade 1, 2, and 3 LTH, respectively (P ⬍ .001)
snoring louder than 45 dB, 38.5% (21.1%-63.8%). Thirty- (Figure 3).

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Table 1. General Characteristics of Patients According to AHI

Severity of OSA, Median (IQR)


Snoring Mild Moderate
(AHI ⬍5/h) (AHI ⱖ5/h to ⬍15/h) (ⱖ15/h to ⬍30/h) Severe (AHI ⱖ30/h)
Variable (n = 12) (n = 30) (n = 35) (n = 20) P Value
Age, y 49.5 (43.0-54.5) 49.0 (42.7-54.5) 54.0 (48.0-59.0) 53.0 (46.5-58.0) .25
Female sex, No. 6 3 3 1 .005 a
BMI 23.4 (21.2-24.6) 24.4 (22.8-26.5) 25.9 (24.3-26.8) 26.6 (25.7-28.4) .001
AHI, h 2.4 (0.5-3.5) 8.7 (6.4-10.5) 22.4 (17.8-26.2) 35.6 (33.0-47.2) ⬍.001
Supine AHI, h 3.5 (0.9-5.6) 14.2 (9.7-19.8) 30.6 (26.4-45.8) 55.6 (41.7-70.1) ⬍.001
ODI, h 0.8 (0-1.2) 4.4 (3.3-6.3) 14.8 (11.3-18.0) 29.8 (23.1-43.2) ⬍.001
SaO2 nadir, % 92.0 (89.0-93.0) 87.5 (86.0-89.0) 84.0 (81.0-85.0) 77.0 (73.0-81.7) ⬍.001
Snoring loudness, dB 45.5 (42.2-49.0) 44.5 (43.0-48.2) 47.0 (44.0-52.0) 48.5 (46.0-52.0) .03
% Snoring ⬎45 dB 30.2 (3.5-54.0) 31.8 (15.5-47.8) 51.1 (27.1-74.7) 52.7 (35.4-76.0) .02
Thickness of LTs, mm b 4.4 (2.5-6.2) 4.4 (2.8-5.3) 4.1 (2.3-5.5) 5.3 (2.5-7.0) .74
Reflux finding score ⬎7, 6 7 9 10 .10
No.

Abbreviations: AHI, apnea hypopnea index; BMI, body mass index (calculated as weight in kilograms divided by height in meters squared); IQR, interquartile
range; LTs, lingual tonsils; ODI, oxygen desaturation index; OSA, obstructive sleep apnea; SaO2, oxygen saturation.
a Fisher exact test.
b Thickness of LTs stands for the mean thickness of midline and paramidline LTs.

Table 2. Agreement Between Endoscopic Findings and Lateral Radiographic Findings on the Hypertrophy of the Lingual Tonsils a

Endoscopic Findings
Lateral Radiography Grade 1 Grade 2 Grade 3 Total
Grade
1 35 8 0 43
2 1 27 3 31
3 0 5 18 23
Total 36 40 21 97

a Cohen ␬ coefficient = 0.731 (P ⬍ .001).

MULTIVARIATE ANALYSES PREDICTING LTH


10
Through multiple stepwise regression analyses, signifi-
cant predictor parameters affecting the thickness of the
Thickness of LT on MRI, mm

8
lingual tonsils measured by MRI were identified
(Table 3). Among demographic characteristics, age and 6
sex did not have significant effects on LTH, but BMI sig-
nificantly affected lingual tonsil thickness (standard- 4
ized ␤ coefficient = 0.189; P = .046). All respiratory vari-
ables, such as AHI, AHI in supine position, minimal 2
oxygen saturation, and loudness and proportion of snor-
ing, did not appear to have any significant effects on LTH. 0
Grade 1 Grade 2 Grade 3
Another significant variable affecting the lingual tonsil
Hypertrophy of LT on Endoscopy
thickness as measured by MRI was a reflux finding score
of 7 or greater (standardized ␤ coefficient = 0.381;
P ⬍ .001). Figure 3. The thickness of the lingual tonsils (LTs) measured on magnetic
resonance imaging according to the endoscopic grades of lingual tonsil
hypertrophy (P ⬍ .001). On each box, the central mark is the median, the
DISCUSSION edges of the box are the first and third quartiles, and the whiskers extend
to the most extreme data points.

The lingual tonsils are known to be one of the anatomi-


cal structures involved in the pathogenesis of OSA.12,13 paring children with persistent OSA after adenotonsil-
So far, most of the studies about the lingual tonsils have lectomy and children without OSA after the same sur-
been done in children.6,8,14-16 The enlarged lingual ton- gery, the prevalence of measurable lingual tonsils was
sils are not uncommon and are sometimes a treatable cause significantly higher in children with OSA than in those
of OSA, particularly in children with Down syndrome who without OSA.15 A case series of 26 children with poly-
already underwent adenotonsillectomy.8 In a study com- somnography-proven persistent OSA after adenotonsil-

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also showed that body mass index was independently as-
Table 3. Multiple Linear Regression Analysis Predicting sociated with lingual tonsil thickness.
the Thickness of the Lingual Tonsils a Our study showed that the endoscopic grading of the
lingual tonsils significantly agreed with the radio-
Standardized
Variable ␤ Coefficient tb P Value
graphic grading on the skull lateral view. In addition, the
quantitative measurement of the lingual tonsil thick-
Age ⫺0.172 ⫺1.864 .07
ness on MRI results was also correlated with their endo-
Sex 0.098 0.970 .33
Body mass index 0.189 2.021 .046
scopic grading. Therefore, in real clinical settings, be-
AHI 0.077 0.750 .46 cause MRI is very expensive and not feasible for patients
Supine AHI 0.030 0.305 .76 with OSA, endoscopic evaluation may provide informa-
SaO2 nadir 0.020 0.201 .84 tion enough to diagnose LTH.
Loudness of snoring 0.053 0.555 .58 To validate the results of our multivariate analyses
% Snoring ⬎45 dB 0.043 0.453 .65 showing that LTH is associated with laryngopharyngeal
Reflux finding score ⬎7 0.381 4.072 ⬍.001
reflux and BMI, further studies should be pursued to show
Abbreviations: AHI, apnea hypopnea index; SaO2, oxygen saturation.
the effects treatment of reflux and BMI has on the hy-
aF = 4.084 (P = .046); df 1 = 1, df 2 = 94; R = 0.423, R 2 = 0.179, adjusted pertrophy of the lingual tonsils.
R 2 = 0.161. Our study has several limitations. First, instead of volu-
b Calculated from t distribution.
metric analyses, simple 2-dimensional thickness of the
lingual tonsils was measured using MRI. In the future,
lectomy showed that the second stage of lingual tonsil- volumetric analyses may reveal an association of LTH with
lectomy decreased the respiratory distress index from 14.8 OSA severity. Second, laryngopharyngeal reflux was not
to 8.1.14 diagnosed through the use of 24-hour esophageal pH
The lingual tonsils may get hypertrophied in a com- monitoring. However, our study also showed signifi-
pensatory manner after palatine tonsillectomy. A study cant associations similar to studies that had performed
showed that children without the palatine tonsils (due to 24-hour pH monitoring.
previous tonsillectomy) had a higher prevalence of the mea- In conclusion, this study showed that reflux finding
surable lingual tonsils than those with the palatine ton- score and BMI were significantly associated with LTH in
sils (78% vs 22%).8 Other causes have also been pre- adults with sleep-disordered breathing, whereas the re-
sented as possible causes of LTH such as laryngopharyngeal spiratory parameters were not associated with LTH. Though
reflux,7 obesity,8 and use of medications such as phe- the measurement of the lingual tonsils was not volumet-
nytoin.9 To our knowledge, there have been a few studies ric and laryngopharyngeal reflux was not diagnosed by a
systematically demonstrating important factors affecting more objective method, our multiple regression analyses
LTH in adults with sleep-disordered breathing. The hy- of demographic, respiratory, radiologic, and endoscopic
pertrophied lingual tonsils obstructing the hypopharyn- findings demonstrate the association of the important fac-
geal airway is also one of the factors leading to the treat- tors with LTH after adjusting for confounders. Further sys-
ment failure of pharyngeal surgery in adults with OSA.17 tematic studies are required to identify the clinical signifi-
Our multivariate analyses showed that the thickness cances of LTH in adults by showing surgical improvement
of the lingual tonsils was significantly associated with re- after lingual tonsillectomy in OSA. In addition, more stud-
flux finding score. A 3-sensor pH study also showed that ies are also required to obtain epidemiologic data of LTH
nasopharyngeal reflux events were more prevalent in pa- in general population and to more clearly identify the re-
tients with severe LTH than in those with mild or mod- lationship of LTH with OSA severity.
erate LTH.18 To our knowledge, the first article that ana-
lyzed the relationship of LTH with OSA in a large Submitted for Publication: October 30, 2012; final re-
population of adult patients was recently published.7 Lin- vision received January 30, 2013; accepted March 21,
gual tonsil hypertrophy was not found in adults with- 2013.
out laryngopharyngeal reflux or OSA, and LTH was larger Correspondence: Jeong-Whun Kim, MD, PhD, Depart-
in patients with laryngopharyngeal reflux and/or OSA than ment of Otorhinolaryngology, Seoul National Univer-
in those without either disease.7 The mechanism of the sity College of Medicine, Seoul National University Bun-
association between laryngopharyngeal reflux and LTH dang Hospital, 166 Goomi-ro, Bundang-gu, Seongnam
is not known. Given that the laryngeal mucosa is dam- 463-707, South Korea (kimemail@naver.com; kimemail
aged by gastric acid and pepsin,19 the lymphoid tissues @snubh.org; kimemail@snu.ac.kr).
of the lingual tonsils might also be damaged and in- Author Contributions: All authors had full access to all
flamed by gastric acid and pepsin. The relationship be- the data in the study and take responsibility for the in-
tween laryngopharyngeal reflux and LTH was also pres- tegrity of the data and the accuracy of the data analysis.
ent in children.20 In contrast, our multiple regression Drs Sung and W. H. Lee contributed equally to this ar-
analyses did not show any significant association of lin- ticle. Study concept and design: Sung, C. H. Lee, and J.-W.
gual tonsil thickness with respiratory events such as AHI, Kim. Acquisition of data: W. H. Lee. Analysis and inter-
oxygen desaturation, and snoring parameters. Al- pretation of data: W. H. Lee, Wee, E. Kim, and J.-W. Kim.
though the palatine tonsils are important factors in caus- Drafting of the manuscript: Sung, W. H. Lee, Wee, E. Kim,
ing OSA, their size is not necessarily associated with OSA and J.-W. Kim. Critical revision of the manuscript for im-
severity,21,22 and also, the thickness of the lingual tonsils portant intellectual content: C. H. Lee and J.-W. Kim. Sta-
is not likely to be associated with OSA severity. Our study tistical analysis: W. H. Lee. Administrative, technical, and

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material support: Wee. Study supervision: Sung, C. H. Lee, 11. Belafsky PC, Postma GN, Koufman JA. The validity and reliability of the reflux
finding score (RFS). Laryngoscope. 2001;111(8):1313-1317.
and J.-W. Kim.
12. Abdel-Aziz M, Ibrahim N, Ahmed A, El-Hamamsy M, Abdel-Khalik MI, El-Hoshy
Conflict of Interest Disclosures: None reported. H. Lingual tonsils hypertrophy; a cause of obstructive sleep apnea in children
after adenotonsillectomy: operative problems and management. Int J Pediatr
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