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DOI: 10.

1051/odfen/2018044 J Dentofacial Anom Orthod 2018;21:106


© The authors

OSAHS in adolescents: clinical presentation


and differential diagnosis
N. Beydon
APHP, Respiratory and Sleep Functional Exploration Unit, Armand Trousseau Hospital, France,
INSERM U938, Saint-Antoine Research Center, Paris, France

ABSTRACT
Adolescent experiment widespread changes as he/ she goes through this transitional period from
childhood to adulthood. Sleep is no exception to this changeover with, as consequences, modifications
of the clinical pre- sentation of subjects with Obstructive Sleep Apnea- Hypopnea Syndrome (OSAHS)
and potential different alternative diagnosis.

KEY WORDS
Obstructive Sleep Apnea-Hypopnea Syndrome (OSAHS), adolescent, diagnostic

The characteristics of obstructive sleep What is the relationship between child-


apnea–hypopnea syndrome (OSAHS) in ad- hood and adolescent OSAHS? How does
olescents are poorly known because of the the upper respiratory tract (URT) and sleep
scarcity of research on the same. The most patterns change during adolescence? What
frequently asked questions are related to are the specific symptoms of adolescent
the risk factors and the clinical and phys- OSAHS?
iological specificities of sleep at this age.

WHAT IS THE RELATIONSHIP BETWEEN CHILDHOOD OSAHS AND


ADOLESCENT OSAHS
Simple snorers children aged 6–13 years who ­ underwent
polysomnography (PSG), 161 children were
Before examining the relationship b
­ etween identified as simple snorers, (SS) which
childhood and adolescent OSAHS, it is worth- means that the PSG showed an absence of
while to consider how snoring develops OSAHS7. Seventy-four of these 161 simple
among children, because OSAHS is o ­ften snorers were re-evaluated 4.6 ± 0.6 years
accompanied by snoring. In Hong Kong,
­ later and it was found that 30% of them
from a general population of 619 C ­ hinese remained SS, 25% presented with ­neither

Address for correspondence:


Nicole Beydon – Hôpital Armand Trousseau
26 Avenue du Docteur Arnold Netter – 75012 Paris Article received: 27-06-2017.
E-mail: nicole.beydon@aphp.fr Accepted for publication: 29-07-2017.

This is an Open Access article distributed under the terms of the Creative Commons Attribution
License (http://creativecommons.org/licenses/by/4.0),
which permits unrestricted use, distribution, and reproduction in any medium,
provided the original work is properly cited. 1

Article available at https://www.jdao-journal.org or https://doi.org/10.1051/odfen/2018044


N. BEYDON

snoring nor OSAHS, and 35% had an either in c­hildhood or adolescence or


apnea–hypopnea index (AHI) of >1/h, quite s­ imply due to a change in the body
whereas only 7% presented with a mass index (BMI) trajectory pattern.
moderate to ­severe OSAHS (AHI ≥ 5/h). In two studies, the clinical signs (in-
These results indicate a good prognosis cluding snoring) in childhood did not
of SS in children, with a low likelihood of constitute a risk factor of OSAHS in
progression to OSAHS in adolescence. adolescence4,12. In the Spilsbury et al.12
study, a medical history of adenoid-
Follow-up of children with or ectomy or tonsillectomy performed
without OSAHS from childhood ­before the first recording (n = 35) or
to adolescence between the two recordings (n = 24)
was a risk factor for the development
Three prospective cohort studies of OSAHS in adolescence even after
aimed at North American populations BMI adjustments were made. Goodwin
among which the majority of subjects et al.4 ­focused specifically on the effect
were identified as at-risk (premature of having a tonsillectomy between the
babies and ethnic minorities, particular- two recordings. Among these chil-
ly black ethnicity) have recently estab- dren who underwent the procedure
lished the link between childhood and between the two PSGs, adolescents
adolescent sleep disorders1,4,12. This had a higher incidence of OSAHS (de-
was achieved by monitoring children fined as a low AHI threshold ≥1) than
with an average age of 4.6–8.4 years the younger children in the population
old from whom two PSG recordings (30% versus 10%, respectively) and
were taken (the first one in early child- their rate of OSAHS remission was also
hood and the second one during adoles- lower. In summary, ENT surgical inter-
cence). The primary findings of these vention appears to be a predisposing
studies are summarized in Table  1. It factor for adolescent OSAHS, thereby
is interesting to note the differences supporting the hypothesis that children
in frequency of detection, remission, who are operated on for adenoid or
and incidence of OSAHS depending on tonsillar hypertrophy because of clinical
whether or not mild OSAHS (AHI 1–5/h.) symptoms of OSAHS would have oth-
is included in the OSAHS group. Nota- er risk factors for OSAHS. These clinical
bly, almost all of the instances of mod- symptoms begin from childhood, high-
erate to severe childhood OSAHS cas- lighted by tonsillar hypertrophy, which
es (AHI between 5 and 10/h or >10/h is almost physiological in young chil-
respectively) had regressed by the dren, or appearing after the operation
time the second recording was done in (constant weight gain after tonsillecto-
adolescence. my)..
The second interesting point of these The influence of the subjects’ ethnici-
studies is the study of the risk factors ties was also evaluated in these studies
for OSAHS in adolescence among because of the heterogeneity of the eth-
these children. The three studies iden- nic groups studied and their frequency
tified statistically significant risk factors in relation to the total population. How-
such as male sex, being overweight ever, a study with the ­majority of black
in terms of true ­obesity, which began subjects (36.5% of the entire population

2 Beydon N. OSAHS in adolescents: clinical presentation and differential diagnosis


OSAHS in adolescents: clinical presentation and differential diagnosis

studied), who are conventionally con- and overweight/obese individuals—


sidered to be predisposed to develop which are not the same risk factors
OSAHS, revealed that belonging to this for childhood OSAHS. Black ethnicity
ethnic group constitutes a risk factor for also appears to affect all ages, whereas
the development of OSAHS in adoles- having an ENT surgical history is rare-
cence (after BMI adjustments)12. ly reported as a predisposing factor
It is evident that the risk factors for in adults. Therefore, it is conceivable
adolescent OSAHS are quite similar to that physiological factors underlie this
those for adult subjects—i.e., males change in risk factors for OSAHS.

PHYSIOLOGICAL MATURATION OF URT AND SLEEP PATTERNS


the ventilatory control that stimulates
URT physiological evolution the pharyngeal respiratory muscles. It
is a known fact that in healthy adults, to
The occurrence of OSAHS involves
prevent the collapse of URT during non-
abnormalities of the two mechanisms
REM sleep, an average negative nasal
that are responsible for the patency of
pressure of −13.3 ± 3.2 cm H2O10 is re-
URT during sleep. These mechanisms
quired, whereas in adults with OSAHS
are (i) the anatomical component in-
an average positive nasal pressure
cluding compliance or collapsibility of
of (+3.3 ± 3.3 cm H2O) is sufficient11.
URT; (ii) the neurogenic component of
This difference is due to the elevated

Table I: The follow-up of three cohorts from childhood to adolescence1,4,12


Initial Follow-up Remission Incidence

Recordings (n)1,4,12 700/503/907 319/319/490


Children
Adolescents
Average delay between the 8.4/4.6/8.2 years
2 recordings1,4,12
Average age (range) 8.5–9.5 (6–12) years 13.7–17.7
(10–23) years

Obesity 12%–15% 15%–19%


SS 15%–21% 9%–25% 31%–60% 4%–25%
Sleepiness* 16% 15% 64% 12%
Apneas observed* 5% 2% 84% 1%

Insomnia* 30% 25% 48% 17%


AHI ≥1/h 11%–24% 15%–30% 52%–70% 10%–27%
AHI ≥5/h 1%–5% 4%–22% 91%–100% 4%–11%
Passage from SS to OSAHS with AHI
≥ 1/h. = 26%, to AHI ≥ 5/h. = 12%
SS: simple snorer; AHI: apnea–hypopnea index, OSAHS: obstructive sleep apnea–hypopnea syndrome
* signs reported in only one of the three studies4.

J Dentofacial Anom Orthod 2018;21:106 3


N. BEYDON

compliance (or increased collapsibility) control16. Nonetheless, the effect of


of URT in adults with OSAHS and trans- weight on the relationship between
lates to a more significant transrespira- ventilatory control and OSAHS cannot
tory pressure gradient in adults with be deduced because normal-weight
OSAHS. In healthy children aged 11 ± adolescents with OSAHS were not in-
3 (≤16) years, it has been shown that cluded in the study.
the slope of the straight line of nasal
transrespiratory pressure–air flow rela- Changing sleep patterns in
tionship during sleep was much lower adolescence
than that of healthy adults, in favor of
a decreased physiological collapsibility It is a well-known fact that physio-
of URT, which is most likely attributable logical sleep changes with age, both in
to the relationship between ventilatory its structure and in its overall duration
control and respiratory compliance8. and rhythms. Regarding the structure,
What about the collapsibility of URT during adolescence, there is a slight
­
in adolescents? Few studies have been decrease in slow-wave sleep with a
conducted, and there is a lack of data concomitant increase in light sleep,
regarding thin children. One study con- while the durations for REM sleep re-
ducted with 27 adolescents, among main stable.
whom seven had OSAHS, showed a The occurrence of obstructive respira-
slope of relationship between transres- tory episodes is rare in healthy children
piratory pressure–air flow during sleep or adolescents, and no link has been
that was higher in adolescents with found between AHI (equal to median
OSAHS, which provides arguments for [range] 0 (0–0.9)/h.) and the age or the
a mixed mechanism—anatomical and pubertal development in 68 healthy,
neurogenic3. nonobese children or adolescents
However, it was found that adoles- (8–18 years; on average ± SD 13 ± 3
cents with OSAHS had a significant- years)13. It can be surmised that there is
ly higher BMI than control subjects no link because obstructive events are
(median [range]: 2.5 [1.7–3.0] versus rare in healthy subjects. There is reason
0.7 [−3.8–2.7] z scores respectively; to believe that if there were subclinical
p < 0.001). Thus, it is difficult to pin- periods of flow limitation in healthy chil-
point what contributes to the phys- dren, they would more frequently lead
iological maturation of the possible to microarousal and/or desaturation
consequences of excess weight or in the healthy adolescent (they would
obesity. However, with regards to the then develop an AHI, which would in-
neurogenic aspect (ventilation control), crease with age) because of the fol-
obese adolescents with OSAHS expe- lowing: (i) the physiological increase in
rienced a hypercapnic ventilatory re- the number of microarousals2 and the
sponse with a similar level of arousal decrease in the cortical microarousal
as obese and thin adolescents who do threshold during obstructive respira-
not have OSAHS, though their ventila- tory events between childhood and
tory response was lower during sleep. adulthood9; (ii) increased collapsibility
This finding thereby indicates an incon- of URT in adolescents (which is simi-
sistent effect of obesity on n­ eurogenic lar to that of adulthood), increasing the

4 Beydon N. OSAHS in adolescents: clinical presentation and differential diagnosis


OSAHS in adolescents: clinical presentation and differential diagnosis

a­ irflow limitation for the same respira- by school rhythms, because schools
tory effort (even nasal pressure) with do not start classes later to cater to
possible desaturation. adolescents. Owing to delayed sleep
In addition to the stabilization of AHI, phase syndrome, adolescents create a
changes in circadian rhythm are sig- sleep deficit during the week for which
nificant in adolescence and are often they can only partially compensate on
the cause of a delayed sleep phase weekends. As a result, there is often
syndrome with delayed physiological a chronic sleep deficit in adolescents.
drowsiness (delayed melatonin secre- In adults, chronic sleep deprivation is
tion) and late spontaneous awakening an aggravating factor of OSAHS and
(the necessary sleep time not being that promotes weight gain. The influence of
different from that of an older child)5. adolescent sleep deficit on the onset of
These modifications are increased by OSAHS is poorly understood.
the increasingly prolonged exposure to All these data can guide the clinician,
light sources in the evenings. Circadian confronted with an adolescent or their
modifications are more severe if blue- family complaining about the subject’s
light (from screens) exposure is high, sleep patterns, to distinguish between
which has led to the availability of soft- those symptoms which are likely to
ware/apps allowing the automatic ac- lead to OSAHS and those related to
tivation of blue-ray filters according to physiological sleep as regards the ad-
the time of day. olescent’s specific lifestyle at that age.
Moreover, this delayed sleep phase
syndrome is not taken into account

CLINICAL SIGNS OF ADOLESCENT OSAHS


First of all, the presence of the previ- In the final analysis, out of 234 children
ously explained risk factors for OSAHS recorded (16%), 38 adolescents were
will more likely result in its diagnosis included, 34.2% of whom were thin,
when dealing with an overweight or 13.2% were overweight, and 53.6%
obese boy, especially if the weight gain were obese. BMI seems to be a risk
took place after the child attained pri- factor in adolescents, in whom OSAHS
mary school age. Once again, because risk is increased 3.5 times for each
of the paucity of information published standard deviation (+1 z-score) in ex-
about adolescents, it is difficult to get cess of the normal BMI range6. Cauca-
an exact idea of the frequency and pro- sian subjects were exclusively included
file of thin adolescents with OSAHS. in this study to avoid the known influ-
In a cross-sectional study in which ence of ethnicity.
relationship between BMI and OSAHS Let us now discuss the symp-
was studied in Caucasian children toms most frequently found in obese
aged 2–18 years, it was necessary to OSAHS adolescents. A study with a
increase the inclusion period to obtain restricted sleep recording (only a nasal
a greater number of adolescents (≥12 cannula + pulse oximetry to facilitate
years) because this population does apnea scoring) of obese population
not frequent sleep centers very often6. of adolescents, distinguished three

J Dentofacial Anom Orthod 2018;21:106 5


N. BEYDON

groups according to the frequency of In summary, according to our current


recorded apneas: no OSAHS (n = 24), knowledge, adolescents with OSAHS
mild OSAHS (apnea index (AI) between are more likely to be obese boys or ad-
2–5/h; n = 29), and moderate to severe olescents who have gained too much
OSAHS (AI ≥5/h; n = 8)14. The follow- weight in recent years, snorers (but not
ing symptoms increased in frequency necessarily from childhood) with pos-
as per AI: snoring, shortness of breath sible breathing difficulties or reported
while sleeping, cessations in breathing nocturnal apnea. Affected adolescents
(apnea) noticed by loved ones, bed-wet- also present with symptoms of depres-
ting, daytime fatigue, and behavior dis- sion, impaired executive functioning
orders. The following signs were not and social skills, or even attention dis-
statistically different among the three orders. The problem is differentiating
groups: restless sleep, the Epworth adolescents with OSAHS from those
Sleepiness Scale scores, morning who are brought in for consultation by
headaches, learning and concentration their families or schools because they
disorders, sleepwalking, nightmares, present with similar symptoms such
tonsillectomy, mouth breathing, aller- as: daytime sleepiness, declining aca-
gies, asthma, smoking, and gastro- demic performance, relationship disor-
esophageal reflux disease (GERD)14. ders (some tend to be reclusive while
Another study conducted on a larger others engage in risky behavior), in ad-
sample, using more sensitive neu- dition to possible drug or alcohol use
robehavioral testing and a complete that can affect sleep. Among these ad-
PSG recording, compared 38 obese olescents, other causes which may ex-
adolescents with OSAHS (AHI ≥ 5/h) plain these neurobehavioral disorders
to 21 obese patients without OSAHS should be sought.
(AHI <1.5/h) and 36 thin adolescents First, delayed sleep phase syndrome
SS (without OSAHS)15. The parental which can lead to fatigue even daytime
assessment showed more cognitive– sleepiness and can be responsible for
behavioral disorders (executive func- both concentration issues as well as
tions, attention, behavioral disorders) neurobehavioral disorders. In addition,
in the obese group with OSAHS than lack of sleep leads to dietary disruptions
in the other two groups, and the ado- that promote weight gain (increasing
lescents’ responses to different ques- the quantity of snacks as well as one’s
tionnaires made it possible to detect appetite for sweet and fatty foods).
more instances of depression and As previously mentioned, weight gain
sleepiness (but only in black subjects). is often considered as an indicator for
Adolescence represents an age when OSAHS. This phase shift will be high-
brain development is still in progress. lighted during history taking (sleep and
Thus, the impact of these disorders on waking hours during the holiday period)
the subsequent behavior of the adult or by having the adolescents maintain
­subject is a question posed by the au- a sleep diary or wear an actimeter for a
thors of the study, who advocate treat- few weeks to objectively test it.
ing the adolescent’s OSAHS so as to Second, it is necessary to eliminate
prevent unfavorable neurobehavioral habits that decrease sleep time, such
changes15. as the use of screens in the evening,

6 Beydon N. OSAHS in adolescents: clinical presentation and differential diagnosis


OSAHS in adolescents: clinical presentation and differential diagnosis

as they have an excitatory effect due to the night to be able to participate in


their content; in addition, as mentioned game play. These behaviors are the di-
above, they cause a delay effect on me- rect result of recent societal changes
latonin secretion because of blue-light and can of course be associated with
exposure. In young individuals indulg- a delayed sleep phase syndrome and
ing in online gaming, it may be the case perhaps even true OSAHS.
that they reschedule wakeful times in

CONCLUSION
Adolescent OSAHS is poorly studied likely have nocturnal respiratory symp-
and almost exclusively described in toms whose neurobehavioral conse-
obese, male adolescents. However, quences are sometimes the only ones
neither excess weight nor the individu- known and can easily be blamed for
al’s sex are risk factors among younger changes inherent in this age group.
children. These changes in risk factors Therefore, clinicians must be cognizant
reflect the anatomical maturation of of how to make such a diagnosis, which
URT and of their neurogenic control. can only be confirmed by a PSG
Adolescents with OSAHS will most
­
­recording.

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