The effects of adenoidectomy on the smell perception of children

Marco Aure´ lio Fornazieri, MD, PhD1,2,3, Rafael Goulart Arau´ jo, MD1, Joa˜ o Vitor Fernandes
Lima1, Felipe Bays Favareto1, Fa´ bio de Rezende Pinna, MD, PhD3, Richard Louis Voegels, MD,
PhD3 and Richard L. Doty, PhD, FAAN4

Background: In this study, we employed a novel

confidence interval [CI], 39.1% to 64%). Improvement on 9
children’s olfactory test in order to more accurately assess
of the 11 odors was present, with significant differences
the re- lationship between nasopharyngeal obstruction
oc- curring for the odors of bubble gum, baby powder,
and odor identification ability. We quantified the impact of
mint, and cinnamon. No sex differences were evident.
ade- noidectomy on olfactory function, established
whether the influences of the operation were related to
Conclusion: Olfactory dysfunction occurs primarily in
the preoper- ative amount of nasopharyngeal obstruction,
chil- dren whose nasopharyngeal obstruction is >50%.
and deter- mined whether sex influenced the olfactory
Removal of the hypertrophied adenoids returned smell
measures.
function back to normal in these cases. This study suggests
that smell loss may be of value in decisions regarding
Methods: Fifty-three boys and 23 girls were administered
whether or not to perform adenoidectomy in children
a standardized children’s olfactory test, the Pediatric Smell
with nasopha- ryngeal obstruction. §C 2018 ARS-AAOA,
WheelTM, before and 45 days after adenoidectomy. They
LLC.
ranged in age from 5 to 12 years and exhibited varying de-
grees of adenotonsillar hypertrophy and histories of recur-
Key Words:
rent adenotonsillitis. Radiographs of the nasopharynx
adenoids; adenoidectomy; smell; olfaction disorders;
were used to grade the degree of nasopharyngeal olfactory perception; sex; diagnostic tests
obstruction.

Results: Significant postoperative improvement in smell How to Cite this Article:

function occurred more frequently in children with >50% Fornazieri MA, Arau´jo RG, Lima JVF, et al. The effects
preoperative obstruction of the nasopharynx. In this of adenoidectomy on the smell perception of children.
group, average function improved 50.8% after Int Forum Allergy Rhinol. 2019;9:87–92.
surgery (95%

lfaction plays an important role in the nutrition of Received: 26 May 2018; Revised: 7 August 2018; Accepted: 17

O
August 2018 DOI: 10.1002/alr.22209
hildren, impacting the flavor of their foods and sub- View this article online at wileyonlinelibrary.com.
sequent food preferences. In fact, most “tastes” reflect
flavor sensations derived from the entrance of volatiles
from
c foodstuffs to the olfactory epithelium via the
nasopharynx

1
Londrina State University, Londrina, Parana´ , Brazil; 2Pontifical
Catholic University of Parana´ , Londrina, Brazil; 3University of Sa˜ o
Paulo, Sa˜ o Paulo, SP, Brazil; 4Smell and Taste Center, Perelman
School of Medicine, University of Pennsylvania, Philadelphia, PA
Correspondence to: Marco Aure´ lio Fornazieri, MD, PhD,
Department of Clinical Surgery, Londrina State University, 60
Robert Koch Avenue, Londrina PR, Brazil, 86038350; e-mail:
marcofornazieri@uel.br
Potential conflict of interest: R.L.D. receives funding from
the Michael J. Fox Foundation for Parkinson’s Research; he is
a consultant to Acorda
Therapeutics, Eisai Co, Ltd, Merck, and Johnson & Johnson;
he receives royalties from Cambridge University Press, Johns
Hopkins University Press, and John Wiley & Sons, Inc.; he is
also president of, and a major shareholder in, Sensonics
International, a manufacturer and distributor of smell and
taste tests. The other authors have no conflicts of interest
to disclose.

International Forum of Allergy & Rhinology, Vol. 9, No. 1, January 2019 87

 during mastication and deglutition. 1 In addition to
enhanc- ing quality of life, this important sensory
system prevents children from eating rotten food and
inhaling smoke or other toxic gases.2–4
Among potential causes of olfactory loss in children
are allergic rhinitis,5, 6 chronic rhinosinusitis with and
with- out nasal polyps,7, 8 traumatic brain injury, 9 and
olfac- tory epithelial inflammation and damage from
viruses and xenobiotics.10 Another frequent etiology is
adenoid hypertrophy.11–13 Such hypertrophy, along
with hyper- trophied tonsils, commonly leads to
nasopharyngeal ob- struction, resulting in higher
airway resistance, dimin- ished inspiration capacity,
altered ventilatory function, and decreased numbers of
odorant molecules that reach the olfactory receptors. 11,
14
If left unchecked, hypertrophic adenoids impact
craniofacial growth and produce retro- clination of the
upper and lower incisors.15 Importantly, hypertrophic
adenoids can result in persistent mouth breathing and,
in extreme cases, sleep apnea, hyperten- sion, and
stroke later in life. Fortunately, adenoidectomy

88 International Forum of Allergy & Rhinology, Vol. 9, No. 1, January 2019

Adenoidectomy and olfaction of
children
Fornazieri et al.

can decrease age group assessed in this Classification of

Adenoid
nasopharyngeal study, boys also have a nasopharyngeal
obstruction, change smaller upper-airway obstruction
mouth breathers to nose length that also in- creases Age (years), mean ± SD 7.4
Nasopharyngeal
breathers, and can nasal airflow.22, 23 Sex (male), % obstruction was
improve olfactory
function,11–13 as well as Race, % determined from a radio-
sleep patterns,16 White
graph of the nasopharynx
appetite, 12
so- matic Pati at the level where a
Non-white
growth,17 and quality of horizontal
ents line could be drawn between
life.18 SD = standard deviation.
In this study, we and the hard palate and the skull
employed a novel and met base (Fig. 1).13 The
practical 11-odor subjects were divided
hod into 2 groups based upon
identification test
designed to capture the
s their obstruction: those
attention and in- terest of A prospective cohort of 76 whose obstruction was
children in order to more children who were >50% and those whose
accurately assess the re- candidates for obstruction was S50%,
lationship between adenotonsillectomy based the latter being defined
nasopharyngeal
± upon adenotonsillar
= ± hyper- as discrete or moderate
obstruction and odor trophy that either obstruction without
major obstructive
identification ability. We impacted normal
symptoms.24, 25
determined whether the breathing, or was as-
degree of such sociated with recurrent or
obstruction is associated chronic infections, were
with the degree of olfac- consec- utively recruited. O
tory dysfunction, whether Their ages ranged from 5 l
some odors are more to 12 years (mean f
sensitive to the standard deviation [SD] a
obstruction than others, 7.2 2.1 years; Table 1).
c
and whether and to what Over one-half were boys
the degree t
(69.9%). The main ex-
adenoidectomy improves clusion criteria were o
olfactory test scores. The having an upper r
latter was assessed both respiratory tract in- fection y
in terms of the total on the day of the olfactory
number of odorants test, chronic diseases, t
identified as well as the history of head trauma, or e
identification perfor- serious cognitive s
mance for each of 11 impairment. We did not t
constituent target exclude children with The subjects were
odorants. Impor- tantly, palatine tonsil hypertro- administered the
we determined whether phy because there is no Portuguese translation of
boys and girls differed in evidence that this would the Pediatric Smell
obstruction-related impair olfactory function.
olfactory dysfunction, WheelTM (PSW), an odor
The local ethics committee
given that, in the age identifica- tion test
approved the study;
group evaluated, specifically designed to
parents provided signed
craniofacial development assess smell function in
informed consent.
is between 5% and 9% children.4 This 11-odor
larger in boys than in forced-choice test, whose
girls, potentially in- TABLE 7-day test-retest
creasing the likelihood of 1. reliability is 0.70 in
greater nasopharyngeal Patie children,4 is comprised of
airflow in boys despite nt a cardboard wheel or disk
equivalent percentages of data that rotates within an
nasopharyngeal by outer jacket, such that
study only 1 microencapsulated
obstruction.19–21 In the
group “scratch and sniff”
 Adenoidectomy and olfaction of
odorant patch at a a children
time is exposed for l
sampling. Be- low each
patch are 4 multiple- a
choice response
n
alternatives consisting
a
of both words and
pictures. Each odorant l
is re- leased using a y
pencil tip. After s
completion of a test i
item, the disk is s
rotated to the next Statistical analysis was
one. In order to adapt performed using STATA
for the Brazilian software (version 13;
children and to STATA Corp., College
increase test Station, TX). After
feasibility, rose and checking normality by
popcorn smells of the the Shapiro-Wilk test,
original version were the olfac- tory
replaced, respectively, identification test
with baby powder and scores were subjected
rubber tire. Although to analysis of
capable of being self- covariance (ANCOVA)
administered, this test with the between
was adminis- tered by subject fac-
a trained technician tors of group (>50% and
who scratched open
S50% obstruction) and
each stim- ulus and
immediately placed sex (M,
F) and the within subject
the odorized patch
factor of
under the nose of the presurgery/postsurgery.
child who was Age served as the
instructed to sniff. The covariate. Comparisons
response alternatives, between groups (>50%
along with the and S50% obstruction)
pictures, were shown were also made based
and read to each child. on 95% confidence
The test score was the intervals (CIs), means,
number of correct an- and percentage
swers. All participants differences.
were tested A sample size of 23
approximately 30 days participants per group
(range, 15 to 90 days) of differ- ent adenoid
before surgery and sizes who completed
approximately 45 days the study appeared to
(range, 40 to 61 days) provide adequate
after the procedure. power to reject the null
hypothesis if it was to
be rejected. Sample size
S determination was
t based on a clinically
a meaningful
t improvement of 2-point
i mean difference before
s and after surgery, a
t power of 90%, a SD of 2
i points, and an alpha
c level of 5%.
Fornazieri et al.

FIGURE 1. Lateral neck X-ray in a child with adenoid hypertrophy (greater than the 50% obstruction point—white cross—in the horizontal line drawn in black
between the hard palate and the skull base). Arrow indicates the small air passage through the nasopharynx.
 Adenoidectomy and olfaction of
children

R
6.1 [95% CI, 5.4 to 6.8]
e vs mean after
s 9.2 [95% CI, = =
u 8.8 to 9.6)]. Seventy-five
l percent of children in
this last group had a
t clinically significant
s improvement in smell
As shown in Figure 2, the capacity. Indeed, except
PSW test scores of the for the preoperative
children with scores of the
nasopharyngeal >50% obstruction
obstruction S50% had a group, mean test scores
small increase of 15.1% were within the range
(95% CI, 3% to 28.1%) considered normal in
after ade- other studies employing
noidectomy (mean the =PSW for subjects of
before surgery 7.3 a similar age.4
[95% CI, 6.6 to To consider the
7.9]; mean after surgery= possibility that
8.4 [95% CI, 7.9 to 8.9]). improvement may
In this group, 37.5% of have been impacted by
children had significant age, we divided the
improvement in olfaction, children by age in 2
as defined by a 10% or =
groups, and compared
greater increase= in test the test scores of those
scores.26 The scores of between 5 and 8 years
the children whose old to those between 9
presurgical obstruction and 12 years of age.
was >50% were When adenoids
significantly lower occupied S50% of the
preopera- tively than nasopharynx, no age-
those of children whose related differences
presurgical obstruction were found (p 0.13).
was S50% (p 0.02). However, when the
Postoperatively, they obstruction was >50%,
improved by 50.8% (95% improvement was
CI, 39.1% to 64%) and slightly better in the
became equivalent to younger than in the
the scores of the other older children (p =
group (mean before 0.04).
surgery
Fornazieri et al.

FIGURE 2. Comparison of olfactory test score pre-adenoidectomy and post-adenoidectomy related to adenoid hypertrophy grade. Horizontal lines in
boxes represent medians. Edges of boxes reflect the interquartile range. Postoperative medians are in the third quartile (upper edge of the box). The
vertical lines represent ranges. The stars are means.

90 International Forum of Allergy & Rhinology, Vol. 9, No. 1, January 2019

 Adenoidectomy and olfaction of
children
The scores of the boys ssio Thus, prior to surgery, performing
and girls did not differ those children in the adenoidectomy. However,
either before (6.4 [95%
n high obstruc- tion most children with
CI, 5.8 to 7] vs 7.0 [95% In general, the impact of group scored adenoid hypertrophy
CI, 6.3 to 7.7], nasopharyngeal abnormally low on the who undergo ade-
respectively) or after (8.8 obstruction sec- ondary to 11-item PSW olfactory noidectomy begin to eat
[95% CI, 8.5 to 9.2] vs 8.8 hypertrophied adenoids test. After surgery, their better. One reason for this
[95% CI, 8.2 to 9.4]) and tonsils on the abil-
+ ity olfactory function re- benefit is likely
surgery and no to smell has received little
+ turned to the normal postoperative
differences were attention by the pediatric range expected on the improvement in airflow
apparent in terms of the and otolaryngologic basis of other from the oral cavity
degree of postoperative communities. Our study applications of this through the nasopharynx
improvement ( 2.4 points demonstrates that children test.4 Since this to the olfactory receptors,
[95% CI, 1.7 to 3.2] vs with nasopharyngeal beneficial effect of ade- thereby increasing the
1.8 [95% CI, 0.8 to 2.8]). obstruction greater than noidectomy applies flavor of the food. This
The general 50% exhibit significant more frequently to enhancement should be
observations noted for smell loss, whereas this is children with hyper- taken into account by the
the median test scores less preva- lent in children trophy greater than surgeon as a factor in
shown in Figure 2 were whose obstruction is less 50% of the deciding whether or not
mirrored, as would be than this amount. nasopharynx space, to operate.
expected, by the scores surgery done for other Our finding that nasal
on most of the individual reasons, eg, chronic obstruction is not
PSW odorant items adenotonsillitis without influenced by sex goes
(Table 2). Preoperatively, adenoid hypertrophy, against our initial
children in the less severe would be expected to hypothesis. We
na- sopharyngeal have a lesser impact on anticipated, be- cause of
obstruction group the ability to smell. larger cross-sectional
identified the onion, baby Interestingly, this area of the nasopharynx
powder, smoke, mint, and improve- ment was in
cinnamon odorants higher in younger
significantly better than children (below 9 years
the children in the more old) when the
severe obstruction nasopharynx
group. Postoperatively, obstruction was >50%.
those who originally had Older chil- dren have a
the worse obstruction more developed
increased their cognitive capacity
percentage of correct which could increase
answers for 9 of the 11 olfactory performance
odors, with the even when a low
improvement being concen- tration of
statis- tically significant molecules reaches the
for bubble gum, baby olfactory epithelium.
powder, mint, and This factor might
cinnamon. Despite small increase their
trends, no statistically preoperative olfactory
significant identifi- cation capacity,
presurgery/postsurgery also verified in our
differences in the sample (p
individual item test 0.01) and in previous
scores were evident for studies.27 Thus, a
the group whose smaller range of test
nasopharyn- score im- provement
geal obstruction was was possible in the =
older children after
S50%.
surgery.
It is questionable
Dis whether olfactory
dysfunction alone is a
cu valid reason for

International Forum of Allergy & Rhinology, Vol. 9, No. 1, January 2019 91

Fornazieri et al.

TABLE 2. Proportion of each individual odorant correctly identified before and after surgery among patients
with obstruction of nasopharynx greater and less than or equal to 50%

Adenoid S50% % (95% CI) Adenoid >50% % (95% CI)

Odorant Preoperative Postoperative Preoperative Postoperative

Onion 100 (1.00 to 1.00) 100 (1.00 to 1.00) 76.4 (0.54 to 0.99) 76.4 (0.54 to 0.99)
Soap 71.4 (0.26 to 1.17) 100 (1.00 to 1.00) 64.7 (0.39 to 0.90) 94.1 (0.82 to 1.07)
Tire 57.1 (0.08 to 1.07) 85.7 (0.51 to 1.21) 70.6 (0.46 to 0.95) 82.4 (0.62 to 1.03)
Bubble gum 71.4 (0.26 to 1.17) 71.4 (0.26 to 1.17) 47.1 (0.21 to 074) 94.1 (0.82 to 1.07)
Banana 28.5 (−0.17 to 0.77) 28.5 (−0.17 to 0.77) 23.5 (0.01 to 0.46) 35.3 (0.10 to 0.61)
Cherry 28.5 (−0.17 to 0.74) 28.5 (−0.17 to 0.74) 29.4 (0.05 to 0.53) 35.2 (0.09 to 0.61)
Baby powder 100 (1.00 to 1.00) 100 (1.00 to 1.00) 70.6 (0.46 to 0.95) 100 (1.00 to 1.00)
Chocolate 42.9 (−0.07 to 0.92) 14.3 (−0.20 to 0.49) 52.9 (0.27 to 0.80) 41.2 (0.15 to 0.67)
Smoke 100 (1.00 to 1.00) 71.4 (0.26 to 1.16) 64.7 (0.39 to 0.90) 70.6 (0.46 to 0.95)
Mint 100 (1.00 to 1.00) 100 (1.00 to 1.00) 41.2 (0.15 to 0.67) 94.1 (0.81 to 1.07)
Cinnamon 100 (1.00 to 1.00) 85.7 (0.51 to 1.21) 47.1 (0.21 to 0.74) 100 (1.00 to 1.00)

CI = confidence interval.

90 International Forum of Allergy & Rhinology, Vol. 9, No. 1, January 2019


boys than girls of the age
of most of our subjects,
that the impact of the
obstruction on smell
function would be less in
the boys. It is possible
that the relatively small
sex difference in
nasopharynx cross-
section area has no
mean- ingful impact on
the airflow parameters
associated with smell
function. It is also
conceivable that the
generally bet- ter
performance of girls than
boys observed on other
tests of olfactory function
might counteract such an
effect, if present.28
However, given our
relatively small sample
size and the considerable
variability known to be
present in the olfactory
test scores between the
sexes, we may have
lacked sufficient power to
see small effects should
they be present. The data
of this study confirm and
extend the ob- servations
of others that nasal
obstruction is related to
the ability of children to
both identify and detect
odors.11, 12, 29 They
contrast with a single
study noting no
significant association
between nasal
obstruction and
orthonasal odor
identification ability in
children using an adult
odor identification test.13
Unlike earlier work, we
employed a smell test
specifically designed for
the pediatric population,
thereby validating this
unique measuring
instrument in children
with nasopharyngeal
obstruction. We also
performed an item
analysis, finding that
children with the worse
nasopharynx obstruction
Adenoidectomy and olfaction of
children
exhibited most were within the normal by nasopharyngeal
postoperative range. Whether cultural obstruction, it does not
improvement for 4 specific factors are involved ad- dress the impact of
odorants: bubble gum, requires further study, such obstruction on
baby powder, mint, and since previous studies adverse effects of
cinnamon. The basis for have found that olfaction on the flavor of
this is not clear, although cultural factors do foods—a problem of
these odors may be more influence test scores considerable
familiar to children than within the Brazilian consequence to children.
some of the others in test. population.30 It is Retronasal stimulation of
Moreover, other stimulus noteworthy that the the ol- factory system, ie,
factors, such as the replacement of rose and stimulation of the
intensity or clarity of the popcorn smells for, olfactory receptors via
odorants, may vary respectively, baby odorants arising within
somewhat in this test. The powder and tire worked the oral cavity, is
children did not identify well. More than 75% of impacted by
the banana and cherry chil- dren could identify nasopharyngeal
smells well either before or the new smells correctly obstruction,12, 31 an
after the surgery after surgery, a important factor when
although, overall, their percentage considered deciding whether
test scores adequate for a cultural adenoidectomy is
validation. This study appropriate. We did not
has both strengths and exclude patients with
weaknesses. It is the rhinitis. Although this is
first to employ a test a potential limitation of
specifically designed for our method, this may not
children to as- sess the have a strong impact on
influences of our results, since a recent
nasopharyngeal study showed no
obstruction, as well as
to establish which odors
seem most sensitive to
such ob- struction
within a pediatric
population. It clearly
establishes that
nasopharyngeal
obstruction greater
than 50% signifi- cantly
impacts olfactory
function. Although this
is the first study to
address the question
whether such
obstruction- related
olfactory dysfunction
differs between the 2
sexes, a definitive
answer to this question
may require larger sam-
ples with more power
to detect small
differences. While our
work clearly
demonstrates that
orthonasal smell func-
tion, ie, the ability to
smell inhaled odorants,
is negatively influenced
International Forum of Allergy & Rhinology, Vol. 9, No. 1, January 2019 91
Fornazieri et al.

92 International Forum of Allergy & Rhinology, Vol. 9, No. 1, January 2019

 Adenoidectomy and olfaction of
children
difference in odor identification test scores among seem to be different between boys and girls, although ad-
children with rhinitis and controls.32 ditional research is needed to confirm or disconfirm this
point.

Conclusion
In children, olfactory improvement for many individual
odorants is another benefit of adenoidectomy, particularly
when adenoid hypertrophy occupies more than one-half of
the nasopharynx. Olfactory dysfunction secondary to ade-
noid hypertrophy and its improvement after surgery do
not
Acknowledgments
We thank Daiane Silva for assistance in data collection. We
are grateful to Hospital Norte do Parana´ (HONPAR) and
all of the children who participated in this study and their
parents who gave their consent.

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