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Adenotonsillectomy improves sleep and gastroesophageal reflux
ORIGINAL ARTICLE
Adenotonsillectomy improves gastroesophageal
reflux, sleep and quality of life in children with
obstructive sleep apnea syndrome - a pilot study
Adenotonsilectomia melhora o refluxo gastroesofágico, o sono e a qualidade de
vida em crianças com apneia do sono - estudo piloto
Alessandra Caland Noronha1, Veralice Meireles Sales de Bruin1, Pedro Felipe Carvalhedo de Bruin1,
Miguel Ângelo Nobre e Souza1, Roberta de Paula Araújo1, Rosa Maria Salani Mota1, Marcos Rabelo de Freitas1
ABSTRACT
Childhood obstructive sleep apnea (OSA) may be associated with
several clinical consequences such as gastroesophageal reflux.
Objectives: In a prospective study, we evaluated the effects of
adenotonsillectomy on quality of life, polysomnographic measures and gastroesophageal reflux disease in children with OSA.
Methods: Twelve children aged 6 to 12 (8.14 ± 1.75) with adenotonsillar hypertrophy and clinical indication for surgical treatment,
were submitted to adenotonsillectomy. Quality of life was evaluated
by OSA-18. Sleep measures, full night polysomnography and 24
hour esophageal pH monitoring were performed simultaneously.
Results: Increased weight and height were observed 3 months
post adenotonsillectomy. Baseline scores of the OSA-18 scale
were significantly improved after surgery (p = 0.001). Polysomnography showed significant reduction of arousals, increased
amount of REM sleep and reduction of the apnea-hypopnea index. Adenotonsillectomy reduced the percent time distal esophageal pH below was 4 (supine period: 11.6 ± 3.4% vs 3.9 ± 1.7%,
p = 0.005; total period: 7.5 ± 1.6% vs 3.7 ± 1.2%, p = 0.007). Adenotonsillectomy also reduced the duration of the longest gastroesophageal reflux episode during the supine position (p = 0.02).
Conclusion: Adenotonsillectomy significantly improved weight
and height measures, gastroesophageal reflux disease, quality of
life, sleep architecture and respiratory abnormalities.
Keywords: adenoidectomy, gastroesophageal reflux, polysomnography,
sleep apnea syndromes, tonsillectomy.
RESUMO
Apneia obstrutiva do sono (AOS) na infância pode associar-se a
complicações, tais como refluxo gastroesofágico. Objetivos: Estudo
prospectivo dos efeitos da adenotonsilectomia na qualidade de vida,
medidas polissonográficas e doença do refluxo gastroesofágico em
crianças com AOS. Métodos: Avaliamos 12 crianças com idade
entre 6 e 12 anos com hipertrofia adenotonsilar. A qualidade de
vida foi avaliada pelo OSA-18; as medidas de sono por meio de
polissonografia e monitoramento do pH de forma simultânea antes
e após adenotonsilectomia. Resultados: Aumento do peso e da
altura e melhora dos escores do OSA 18 foram observados após
a adenotonsilectomia (p = 0,001). A polissonografia evidenciou
redução dos despertares, aumento do sono REM e redução do índice de apneia e hipopneia. Adenotonsilectomia reduziu a porcentagem de tempo de pH esofágico distal abaixo de 4 (período de
supino: 11,6 ± 3,4% vs. 3,9 ± 1,7%, p = 0,005; período total: 7,5
± 1,6% vs. 3,7 ± 1,2%, p = 0,007). Adenotonsilectomia também
reduziu a duração do maior episódio de refluxo gastroesofágico,
durante a posição supina (p = 0,02). Conclusão: A adenotonsilectomia melhorou significativamente o peso e as medidas de altura,
doença do refluxo gastroesofágico, qualidade de vida, arquitetura
do sono e alterações respiratórias.
Descritores: adenoidectomia, polissonografia, refluxo gastroesofágico,
síndromes da apneia do sono, tonsilectomia.
INTRODUCTION
Obstructive sleep apnea syndrome (OSA) is common in children
and is usually caused by hypertrophied adenoids and tonsils(1,2).
Usually, symptomatic children with hyperplasic or hypertrophied adenoids and tonsils are considered for surgical intervention as treatment of choice. Follow-up after adenotonsillectomy
has shown that these children present lower health care utilization costs, improvement of quality of life, better sleep, and
improved neurocognitive function(3,4). However, persistence of
OSA after adenotonsillectomy has also been shown to occur(5)
and attempts to correlate objective measures of OSA with improvement after adenotonsillectomy have frequently failed(6-8).
Moreover, reduced quality of life, present in these children, does
not correlate with objective measures of OSA suggesting the
involvement of other mechanisms(9).
Gastroesophageal reflux disease (GERD) is frequently
found in association with OSA(10). Attempts to demonstrate a
temporal relationship between gastroesophageal reflux episodes
and apnea-hypopnea events have generally failed(11,12). Several
studies have shown that CPAP therapy improves GERD(13,14)
Study carried out at Universidade Federal do Ceará.
1
Universidade Federal do Ceará.
Corresponding author: Veralice Meireles Sales de Bruin. Pós-Graduação em Ciências Médicas, Universidade Federal do Ceará. Rua Cel. Nunes de Melo nº 1315,
Fortaleza - CE. Brazil. CEP: 60.430-270. Phone: 55 (85) 3242-1681. Fax: 55 (85) 3261-5540. E-mail: [email protected]
Financial Support: MCT/CNPq.
Received: June 29, 2012; Accepted: April 11,2013.
Sleep Sci. 2013;6(2):48-53
Noronha AC, Bruin VMS, Bruin PFC, Souza MAN, Araújo RP, Mota RMS, et al.
and conversely fewer studies have demonstrated an improvement of apnea-hypopnea index (AHI) severity after therapy
with ranitidine or proton bomb inhibitors for gastroesophageal
reflux(15,16). In small children, the association between GERD
and respiratory disturbances seems more consistent and as
both, GERD and OSA are of multi factorial origin, age might
be playing a key role in the manifestation of these symptoms.
It has been previously shown that the beneficial outcome of adenotonsillectomy is not consistently associated with
polysomnographic measures such as a reduction of OSA or improvement of sleep architecture(17). Thus, a better understanding
on how adenotonsillectomy influences the respiratory events,
gastroesophageal reflux and sleep homeostasis is in need.
The aim of this study was to evaluate the effects of adenotonsillectomy on clinical findings, quality of life, polysomnographic
measures and gastro esophageal reflux in children with OSAS.
MATERIAL AND METHODS
Study Population
This was a prospective study of children with clinical indication
of adenotonsillectomy. Inclusion criteria were adenotonsillar
hypertrophy, grades 3 and 4, or adenoids with 70% or more of
occlusion. Exclusion criteria were the presence of neurological
disorders, constitutional maxillofacial anomalies and the use of
sedative or antiepileptic drugs. Demographic and clinical data
were recorded using a closed-question, data collection instrument. All variables and measures were taken at baseline, meaning pre-adenotonsillectomy, and three months after surgery or
post-adenotonsillectomy. Fourteen children of both gender
aged from 6 to 12 years were initially included. Two individuals
did not finish the study. One case had unsatisfactory pH monitoring and one had insufficient data from the polysomnography.
Thus, simultaneous recording, before and after adenotonsillectomy, was performed in 12 children. The study protocol was
approved by the local Research Ethics Committee and written
informed consent was obtained from parents in all cases.
Procedures
Clinical Evaluation
After clinical examination, a previously validated Portuguese version of OSA-18, a questionnaire related to the presence of apnea in childhood, was applied(17). This questionnaire is divided in
five items about sleep disturbance, physical suffering, emotional
distress, daytime problems, and caregiver concerns. Scores vary
from 18 to 126. Scores lower than 60 mean a small impairment
of quality of life, from 60 to 80 moderate impact and greater
than 80 mean a high impairment. A visual analogical scale varying from 0 (bad quality of life) to 10 (good quality of life is
also part of this questionnaire(18). Objective questioning about
several symptoms such as the presence of halitosis, sore throat,
sinusitis, irritable mood, stomach ache, frequent vomiting,
anorexia and hoarseness, between others, was performed.
All children were examined with nasofibrolaringoscopy
for inspection of nasal mucosa, adenoids and tonsils. The degree
of obstruction was graded according to the occlusion as Grade
1 (less than 25% occlusion), Grade 2 (less than 50% occlusion),
Grade 3 (less than 75% occlusion) and Grade 4 (more than 75%
occlusion). Signs of erythema or hyperemia of arythenoids and
vocal cord were also registered.
Polysomnography
Standard overnight polysomnographic recordings (PSGs)
were performed on an ALICE II digital polygraph. PSGs
were set to begin at 10 p.m. (lights-out) and ending at 6
a.m. (lights-on). Monitored variables included electroencephalogram (EEG) (C3, C4, O1, O2 referenced to contralateral ear electrodes), electro-oculograms (EOG),
submental electro-myogram (EMG), two-lead electrocardiogram (ECG) and pulse oximetry. Leg movements were monitored using a bilateral tibialis EMG and respiration using a
nasal/oral thermocouple. Body position and thoracic and abdominal movements (inductance plethysmography) were also
recorded. Sleep staging was performed by 30-s epochs according to standard procedures. Polysomnography-derived parameters evaluated were apnea-hipopnea index (AHI), minimum
oxygen saturation (SaO2), sleep latency, sleep efficiency, REM
latency, amount of REM sleep (% of Total Time of Sleep),
amount of non-rapid eye movement (NREM) sleep (% of
Total Time of Sleep), number of arousals and PLM. Arousal
analysis(19) and scoring of respiratory events(20) during sleep
were performed according to standard criteria. Apneas were
defined as cessation of airflow for 10s or more and hypopneas
as a reduction of inspiratory air flow of 50% or more associated with either oxygen desaturation of > 3% or an arousal.
Severity of sleep-disordered breathing was estimated by calculating the apnea-hypopnea index (AHI; apneas plus hypopneas
per hour of sleep).
Esophageal pH Monitoring
Prolonged esophageal pH monitoring was performed using
antimony pH electrodë with a separate skin reference electrode (Sigma Instruments, Belo Horizonte, Brazil®). The data
were stored on a portable digital recorder (Sigma Instruments,
Belo Horizonte, Brazil). Before each study, the pH probe was
calibrated in buffer solutions of pH 7 and 1. An episode of
acid reflux was defined as a decrease in esophageal pH to less
than 4 during more than 10 seconds. Esophageal pH monitoring lasted for approximately 24 hours. After a 4-hour fast
period, the probe was placed transnasally into the stomach,
and, then, slowly withdrawn in such a way that the tip of
the electrode would lie over the third vertebral body above
the diaphragm(21). Its position was confirmed by a chest Xray. Mealtime, changes in decubitus and occurrence of clinical symptoms were recorded. No nutritional restraints were
imposed on the children during examination. The parameters
analyzed by esophageal pH monitoring included: absolute
and percent total times pH < 4; absolute and percent supine
times pH < 4; absolute and percent upright times pH < 4;
total number of acid reflux episodes; number of acid reflux
episodes while supine, number of acid reflux episodes while
Sleep Sci. 2013;6(2):48-53
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Adenotonsillectomy improves sleep and gastroesophageal reflux
upright; total number of acid reflux episodes > 5 minutes
(while supine and upright); and longest acid reflux episode
during the pH test (while supine and upright).
Surgical Procedure
Surgical procedure was performed under general anesthesia with
the supine patient in Rose position on the operating table. Adenoidectomy was performed in all patients by the same technique.
Digital examination of the nasopharynx confirmed the presence of adenoidal tissue and excluded any abnormal pulsation.
The adenoidal tissue was removed by using appropriate sized
Beckham adenoidal curettes. Then, a nasopharyngeal pack was
placed in the nasopharynx. Cold dissection tonsillectomy was
performed. An Allis clamp was applied to the superior pole
of the tonsil and an incision was made through the anterior
tonsillar pillar to expose the underlying capsule of the tonsil that
was dissected with Hurd dissector-retractor and blunt scissors
from the tonsillar fossa. A swab was placed in the fosse and the
other tonsil was removed similarly.
Data Analysis
Data were examined using the Shapiro-Wilk for normality and
Levene test for homogeneity of variance. Wilcoxon sign-rank test
was used to compare cases pre and post-adenotonsillectomy. Paired
sample t test was used to compare measures of weight and height
pre and post-adenotonsillectomy. Spearman correlation test was
used between improvement of OSA-18, PSG and GERD measures. Statistical analysis was performed with the Statistic Package
for Social Sciences (SPSS- Norusis, 1993) software for Windows.
The level of significance was set at p < 0.05.
RESULTS
Twelve children, seven of male gender (58.3%), aged from six to
12 years old (8.14 ± 1.75) were studied. Adenoid hyperplasia was
present in two (16.6%), tonsillar hypertrophy in 11 (91.6%) and
adenotonsillar hyperplasia in four (33.3%). Generally, larynsgoscope findings improved after surgery (Table 1). Laryngoscope
findings after surgery showed a greater amount of normal tissue and a reduction of macroscopic abnormalities such as
arytenoids edema and hyperemia, and vocal cord nodules. In
one case, a vocal cord polyp was found after adenotonsillectomy. Children weight and height improved significantly after
adenotonsillectomy as compared to before the surgery, over a
three-month period (Weight: 30.25 ± 9.82 kg vs. 27.09 ± 8.34 kg;
height: 1.29 ± 0.11 m vs. 1.24 ± 0.11 m; paired sample t test, p <
0.005). Baseline global scores of the OSA-18 scale were significantly improved after adenotonsilletomy (Wilcoxon, p = 0.001)
(Table 2). Except for emotional symptoms, all other components of the OSA-18 scale showed significant improvement in
relation to pre-adenotonsillectomy values (p < 0.001) (Table 2).
Post-adenotonsillectomy polysomnography showed
a reduction of arousals, increased amount of REM sleep, a
trend for improvement of oxygen desaturation as expressed
by median and minimum SaO2 and a reduction of the
apnea-hypopnea index (Table 3).
Sleep Sci. 2013;6(2):48-53
Table 1. Description of laryngoscope findings pre-and post-adenotonsillectomy.
Pre-adenotonsillectomy
N%
Post-adenotonsillectomy
N%
Normal
4
18.1
7
41.1
Arytenoid edema
13
59.0
8
47.0
Arytenoid hyperemia
9
40.9
5
29.4
Vocal cord nodes
2
9.0
2
9.0
1
5.8
Vocal cord polyps
Adenotonsillectomy leaded to a reduced exposure of the
distal esophagus to acid reflux (Figure 1). Exposure (% time
pH < 4) reduction occurred significantly for the supine (11.6 ±
3.4% vs. 3.9 ± 1.7%, p = 0.005) and total (7.5 ± 1.6% vs. 3.7 ±
1.2%, p = 0.007) periods. There was a nonsignificant exposure
reduction for the post-adenotonsillectomy upright period (4.7
± 0.6 vs. 2.9 ± 1.3, p = 0.054). Besides diminishing acid attack,
adenotonsillectomy also reduced the duration of the longest
gastroesophageal reflux episode during the supine position
(p = 0.02) (Table 4).
DISCUSSION
Our data show that adenotonsillectomy improves quality of life,
sleep polysomnographic measures and gastroesophageal reflux
episodes in children aged from 6 to 12 years old suffering from
OSA. Similar to previous reports, obesity was not found in this
study(1). In fact, some children were under weighted. Of interest, at three months after surgery, children presented significant
improvement of measures of weight and height. Improvement
of quality of life did not correlate with improvement of sleep
variables. Adenotonsillectomy significantly diminished the esophageal acid exposure due to reflux. This finding shows the
importance of diagnosing and treating GERD in children with
OSA and adenotonsillar hypertrophy.
In agreement with other studies and despite the small
sample evaluated, most components of the OSA-18 quality
of life scale were improved after three months of surgery(22).
Sleep disturbance and parental reaction were the most significant ameliorated measures and this is in agreement with
other report(23). Emotional symptoms were not changed in our
study. Previously, it has also been shown that this component
of the OSA-18 scale is less affected in children with OSA and
adenotonsillar hypertrophy and a more pronounced improvement in quality of life in the short-term has also been noticed(24).
In this study, REM sleep and arousals were all improved after adenotonsillectomy in agreement with previous
studies(24). However, a second night effect cannot be excluded. REM latency and percentage of cumulative REM sleep
are some of the measures known to be influenced by a second night effect(24). Our findings of normal sleep efficiency and little change of sleep architecture are in agreement
with a previous description that the increased arousal index
in these children is not associated with major abnormality
in the sleep architecture(25). Our data confirm that disturbed
sleep or restless sleep as described for these children, are
improved by adenotonsillectomy. Apnea-hypopnea index and
Noronha AC, Bruin VMS, Bruin PFC, Souza MAN, Araújo RP, Mota RMS, et al.
Table 2. Comparison of the outcome of OSA-18 components and global scores pre-and post-adenotonsillectomy (Wilcoxon test).
Pre-adenotonsillectomy
Post-adenotonsillectomy
p value
N
Range
Mean
SE
Range
Mean
SE
Global score
12
39-102
77.59
3.74
19-52
36.35
2.18
0.001
Sleep disturbance
12
6-26
18.18
1.29
4-9
4.76
0.32
0.001
Physical symptoms
12
6-21
15.18
1.10
4-9
5.53
0.43
0.001
Emotional symptoms
12
4-21
10.71
1.38
4-20
12.29
1.42
0.2
Diurnal dysfunction
12
5-17
11.35
0.91
3-15
8.06
0.98
0.006
Parental reaction
12
12-28
22.18
1.12
4-15
5.71
0.75
0.001
Quality of life (analogical scale)
12
0-8
4.06
0.52
7-10
8.71
0.25
0.001
Table 3. Comparison of the outcome of polysomnographic test measures pre-and post-adenotonsillectomy.
Post-adenotonsillectomy
Polysomnographic test measures
Range
Mean
Range
Wilcoxon
Mean
SE
p value
Sleep efficiency (%)
84.4-99.8
95.53
87-97.9
91.69
1.01
0.039
Total sleep time(min)
377-527
450.75
444-521
471.46
7.8
0.388
2-55
13.4
4-38
22.8
3.0
0.1
NREM Phase 1 (%)
0.14-1.25
0.5
0.58-2.69
1.3
0.1
0.008
NREM 2 (%)
28.1-68.7
49
25.6-51.29
36.1
2.4
0.006
NREM 3-4
11.3-47.9
30.7
25.3-44.6
35.3
2.1
0.2
REM sleep (%)
12.2-27.3
19.9
19-34.36
26.1
1.2
0.001
69-141
103.4
62-153
99.7
7
0.7
Arousal index (ev/h)
4-45
14.43
1-12
5.55
0.92
0.039
Median SaO2
89-97
94.5
93-97
95.8
0.1
0.09
Minimum SaO2
53-90
80.3
80-89
85.7
0.8
0.07
0.86-38.8
7.6
0.4-4.4
1.9
0.4
0.03
Sleep latency(min)
REM latency (min)
AHI (ev/h)
NREM = Non-rapid eye movement; REM = Rapid eye movement; ev/h = Events/hour; SaO2 = Oxygen saturation; AHI = Apnea-hypopnea index.
Table 4. Comparison of the outcome of pH monitoring pre-and post-adenotonsillectomy.
pH monitoring values
Pre-adenotonsillectomy
Post-adenotonsillectomy
Wilcoxon
Range
Mean
SE
Range
Mean
SE
p value
22-171
75.4
11.7
17-181
55.2
14.3
0.20
0-50
22.4
4.3
0-50
20.1
5.6
0.70
22-125
53.6
8.4
2-148
35.4
11.9
0.60
24h GER > 5 min (N)
0-8
2.3
0.7
0-5
1.3
0.5
0.19
Supine GER > 5 min (N)
0-8
2.0
0.7
0-4
1.0
0.4
0.17
Standing GER > 5min (N)
0-2
0.3
0.2
0-3
0.2
0.2
0.80
24h longest GER (min)
2-84
32.0
9.1
1-95
15.8
8.4
0.02
Supine longest GER (min)
2-84
15.1
8.5
0-95
31.3
9.3
0.02
Standing longest GER (min)
2-8
4.0
0.5
0-11
2.7
0.9
0.24
24h pH < 4/(min)
25-251
113.7
22.3
8-173
48.7
17.1
0.007
Supine time pH < 4 (min)
0-233
68.1
21.3
1-146
32.2
13.7
0.05
Standing pH < 4/(min)
17-83
39.1
5.9
1-113
19.8
9.5
0.09
1.4-17.5
7.5
1.6
0.6-12.1
3.7
1.2
0.01
Supine pH < 4 (% value)
0-35.6
11.6
3.4
0-19.3
3.9
1.7
0.02
Standing pH < 4 (% value)
2.4-10
4.7
0.6
0.3-15.7
2.9
1.3
0.22
24h GER (N)
Supine total GER (N)
Standing GER (N)
24h pH < 4 (% value)
GER = Gastroesophageal reflux; min = Minutes; h = Hour; % = Percent.
oxygen desaturation were also improved after surgery and
these measures can be more accurately diagnosed in first
night studies in sleep disordered breathing(26) and do not
change as a consequence of second night effect as has been
demonstrated in other pathologies(27).
The association between GERD and OSA has been
previously reported in approximately 40% of cases with obesity(28).
In our study, we found GERD to be very common and this high
frequency may be explained by the fact that this was a small
group with severe adenotonsillar hypertrophy with indication for
Sleep Sci. 2013;6(2):48-53
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Adenotonsillectomy improves sleep and gastroesophageal reflux
Figure 1. Adenotonsilectomy reduced the distal esophageal acid exposure due to GER, for the total (p = 0.003), supine (p = 0.002), and upright (p = 0.027) times. The vertical
axis represents the percentage time pH was below 4 before minus after surgery for each individual. The horizontal axis represents the mean of the percentage time pH was below
4 before and after surgery for each individual. Dotted horizontal lines show mean differences and 95% confidence intervals. Points are matched pairs. Wilcoxon Sign-Rank Test,
n = 11.
surgical treatment. In our study and similar to a previous report,
gastroesophageal reflux episodes were not influenced by the body
mass index(28). Our data indicate that esophageal acid exposure
in children with adenotonsillar hypertrophy is greatly a consequence of upper airway obstruction, since adenotonsillectomy reduces acid exposure significantly. It is known that CPAP reduces
gastroesophageal reflux episode in OSA and healthy volunteers,
possibly by increasing esophageal and LES pressure(29). Thus,
CPAP can diminish the pressure gradient between the stomach
and the esophagus. Adenotonsillectomy, may have a similar effect since reducing inspiratory effort during sleep increases
intraesophageal pressure, at least during most inspiratory phases.
CONCLUSION
Adenotonsillectomy, in children from 6 to 12 years of age, significantly
improved weight and height measures, GERD, quality of life as evaluated by the OSA-18, sleep architecture and respiratory abnormalities.
ACKNOWLEDGEMENT
We wish to thank MCT/CNPq for partial support of
this study.
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