Nasal Cytology in the Diagnosis of Allergic

Rhinitis in Children
Article in Annals of allergy, asthma & immunology: official publication of the American College of Allergy,
Asthma, & Immunology · February 2017
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Nasal cytology in the diagnosis of allergic rhinitis
in children
Orathai Jirapongsananuruk, MD* and Pakit Vichyanond, MD*³

Background: Inflammatory cellular infiltrates of eosinophils and basophilic While the release of mast cell media-
metachromatic cells are the hallmark of the atopic nasal responses in allergic tors characterizes the early allergic na-
rhinitis. Nasal cytologic examination for these cells not only establishes the diag- sal response, eosinophils with accom-
nosis of allergic rhinitis but is also useful in the followup of patients with this panying basophils play an important
condition. role in the late phase nasal response.
Objectives: To determine the usefulness of quantitative nasal cytology as an Basophils and mast cells from hu-man
adjunctive diagnostic tool for children with allergic rhinitis in addition to history, nasal scrapings stain basically with basic
physical examination and allergy skin testing. aniline dyes and metachro-matically
Materials and Methods: Forty-eight children with allergic rhinitis less than 15 with toluidine blue, leading to the
years of age were recruited and evaluated for the following variables: symptoms synonymous terms ªbasophilic
and signs of allergic rhinitis, skin prick tests to common aeroallergens, paranasal metachromatic cellsº for both cell
sinus radiographs, and nasal cytology. Forty-one normal and healthy children less types.5 Nasal mast cells can be classi-
than 15 years of age served as controls. Nasal mucosal specimens were obtained by fied by their neutral protease content
scraping the middle one-third of inferior turbinates with Rhinoprobes and were into tryptase-positive, chymase-nega-
stained with Wright-Giemsa stain. Nasal cytology was examined under a light tive (MCT) and tryptase-positive,
microscope and graded according to a previously suggested scoring system. chymase-positive (MCTC) subtypes.6
Results: There were distinctive differences in the scores for nasal eosinophils These subtypes correspond with muco-
and basophilic metachromatic cells between the allergic rhinitis and the control sal and connective tissue mast cells,
groups (P , .001). The sensitivity for nasal eosinophil scores or nasal basophilic respectively. Ultrastructural examina-
meta-chromatic cell scores more than 0.5 in the diagnosis of allergic rhinitis was tion of the allergic nasal mucosa re-veals
91.7% with a specificity of 100%, positive predictive value of 100% and a negative three types of basophilic meta-chromatic
predictive value of 91.1%. Presence of polymorphonuclear cells did not correlate cells localizing in various locations in
with the presence of sinusitis as diagnosed by paranasal sinus radiographs. Nasal the nasal mucosa: (1) ba-sophils
eosinophil scores correlated significantly with sign scores (P 5 .009). House dust predominate on the mucosal surface, (2)
mites were the most common allergens sensitized by this group of children (67.4% MCT cells reside princi-pally in the
to 88.4%). nasal epithelium and, (3) MCTC cells are
Conclusion: Nasal cytology is a quick, simple, and inexpensive tool not only for situated mainly in the deeper lamina
the diagnosis of allergic rhinitis but also for serial evaluations of children with this
propria.7 Basophilic metachromatic cells
condition as well.
obtained by gentle scraping of inferior
Ann Allergy Asthma Immunol 2017;80:165±70.
turbinates consist
of 83% MCT, 10% MCTC, and 7% ba-
INTRODUCTION ber of mast cells in the nasal mucosa
sophils.8 In contrast eosinophils, iden-
Allergic rhinitis, an inflammatory dis- also increases after pollen exposure.1 tified by their affinity for acidic dye
ease of the nose, is characterized by In antigen challenges, a small but sig- eosin for their content of major basic
influxes of eosinophils and basophils nificant increase of eosinophils could protein, are found throughout the nasal
into nasal secretions and nasal mucosa. be observed in nasal lavage fluid mucosa, with the highest density
During natural exposure to allergen, within one hour after the challenge local-izing in the lamina propria.9
eosinophils in nasal lavages increase 20- procedure prior to a dramatic increase Nasal cytology has been utilized as
fold, followed closely by increasing 7 to 11 hours, thereafter.2,3 This late a diagnostic tool in the differentiation
nasal symptoms. In addition, the num- increase of eosinophils is associated of chronic rhinitis in adults. Lee and
with an increase in the number of neu- as-sociates reported that the ratio of
* Division of Allergy and Immunology, De- trophils, basophils, and mononuclear eo-sinophils to neutrophils in the nasal
partment of Pediatrics, Faculty of Medicine cells. A strong correlation between ba- secretions of more than 0.1 is specific
Siriraj Hospital, Mahidol University, Bangkok, sophil numbers and histamine level as for seasonal and perennial allergic rhi-
Thailand.
Accepted for publication in revised form Oc-
well as between eosinophil numbers nitis.10 In children, the usefulness of
tober 28, 2017. and amount of major basic protein was nasal cytology has been examined in a
observed in late nasal reactions.2± 4 limited number of investigations.

VOLUME 80, FEBRUARY, 2017

165
Miller et al examined blown nasal se-
cretions and scraped nasal samples
from children and found nasal eosino-
philia ($4%) in 69% of those with
seasonal allergic rhinitis compared to
only 7% of normal children.11 Jong et
al indicated that polymorphonuclear
cells of $5 per high power field in
specimens obtained by Rhinoprobe
significantly correlated with the pres-
ence of radiographic sinusitis in asth-
matic children.12 These studies
utilized different techniques for cell
collection as well as for cell staining
and are difficult to apply to clinical
usage. Ad-ditional information on
nasal cytology in allergic rhinitis in
children is still needed.
Our objectives are to examine the
nasal cytology in children with
allergic rhinitis and to correlate
cytologic de-grees with clinical
history, physical findings, and with
skin prick test re-sults.
MATERIALS AND METHODS
Children less than 15 years of age with
clinical diagnoses of allergic rhinitis by
history and physical examination and
with positive skin prick tests to a panel
of common aeroallergens were recruited
from the Allergy Clinic, Siriraj Hospital,
Mahidol University, Bangkok, Thailand.
None had received intranasal
steroid/sodium cromogly-cate for 1
month nor oral ketotifen/ second
generation antihistamine for 1 week
prior to enrollment into the study. No
subjects had previously re-ceived oral
steroids or astemizole. Symptoms
(sneezing/itching, nasal congestion,
runny nose, postnasal drip) and signs
(turbinate color and swell-ing, nasal
discharge, and pharyngeal
inflammation) of allergic rhinitis were
scored according to a scoring system
(with score of 0 to 3) as suggested by
Meltzer.13 Allergy skin testing was
performed by the prick method using
bifurcated needles on the upper back.
Panels of common aeroallergens for
Thailand included Dermatophagoides
pteronyssinus, Dermatophagoides fari-
nae, American cockroach, Johnson
grass, Bermuda grass, Timothy grass,
acacia, Penicillium, Aspergillus, corn
166
smut, Alternaria, Cladosporium, Fusar-
ium, cat, dog, and food antigens ie: egg
white, egg yolk, soy, beef, shrimp, crab,
and mixed shellfish (Center Laborato-
ries, Port Washington, NY). Wheals of
$3 mm greater than saline control were
considered positive. Histamine phos-
phate (10 mg/mL) was used as positive
control.
Paranasal sinus radiographs were
obtained from 35 children in the rhini-
tis group and were interpreted by an
experienced radiologist. Criteria for
di-agnosis of sinusitis are complete
opaci-fication of a paranasal sinus,
more than 4 mm thickening of
paranasal sinus mucosa, or more than
25% thickening of mucosa. Of these
35 roentgenologic studies, 26 were
considered positive for sinusitis. High
percentages of pa-tients with sinusitis
in this study reflect the referral nature
of our clinic which accepts only
patients who have been adequately
treated by general pediatri-cians.
Nasal mucosal specimens were ob-
tained, processed, and enumerated as
described in previously reported meth-
ods.13 In brief, mucosal specimens were
scraped from the surfaces of the middle
thirds of inferior turbinates with
Rhinoprobes (Arlington Scientific Inc,
Arlington, TX). They were trans-ferred
onto glass slides, fixed in 95% ethyl
alcohol, and stained with modi-fied
Wright-Giemsa stain. Nasal baso-philic
metachromatic cells and eosino-phils
were enumerated at 31000
magnification under a light micro-scope.
At least 10-well spread, high power
epithelium fields were exam-ined
independently by two allergists, one of
whom was blinded to clinical status of
the patients. The quantitative score of
nasal basophilic metachro-matic cells,
eosinophils and polymor-phonuclear
cells was rated according to a scale
previously described by Meltzer14
(Table 1). The concordance rate for
nasal cytology scores as deter-mined
among the two allergists was 100% for
eosinophils, 95.83% for ba-sophilic
metachromatic cells and 97.92% for
polymorphonuclear cells with
coefficients of variation of 0.89, 0.90
and 0.92 for eosinophils, baso-
ANNALS OF ALLERGY, ASTHMA, & IMMUNOLOGY
Table 1. Semiquantitative Nasal Cytology
Grading Score14
Grading of Cells Grade
Eosinophils, neutrophils
0 0
0.1±1.0* 1/21
1.1±5.0* 11
6.0±15.0* 21
16.0±20.0* 31
.20.0* 41
Basophilic cells
0 0
0.1±0.3* 1/21
0.4±1.0* 11
1.1±3.0* 21
3.1±6.0* 31
.6.0* 41
* Mean of cells per 10 high power field
(31000).
philic metachromatic cells and poly-
morphonuclear cells, respectively (P ,
.0001). Nonatopic, healthy chil-dren
less than 15 years of age with normal
physical examinations were ex-amined
for nasal cytology as control subjects.
Data were analyzed using Mann-
Whitney U tests in the comparison of
cytology scores between control and
allergic rhinitis groups. Correlations
between variables was analyzed by
Spearman rank correlations. All calcu-
lations were performed on a Macin-
tosh II SI computer (Cupertino, CA)
using the Statview IV program (Cala-
bacus, CA).
RESULTS
Forty-eight children with allergic rhi-
nitis were enrolled into the study.
Their mean age was 8.16 6 0.3 years
(range 8.5 to 180 months) with two
children less than 2 years, 22 from 2 to
8 years, and 24 from 8 to 15 years of
age. Forty-one normal children, with a
mean age of 3.75 6 4.0 years (range 1
to 168 months) were enrolled as con-
trols (23 children less than 2 years, 9
from 2 to 8 years, and 9 from 8 to 15
years of age). Median scores for
symp-toms and signs were 5.5 and 7
in the rhinitis group.
The comparison of cytology scores
for eosinophil and basophilic meta-
chromatic cells between control and
Table 2. Number of Patients with Varying Numbers of Nasal Eosinophils (EOS) and
Basophilic Metachromatic Cell (BMC) Scores in Allergic Rhinitis and in Normal Subjects
Number of Patient with EOS
Score Scores
Allergic Rhinitis Control
4 3
3 2
2 12
1 14
0.5 13
0 4
Total 48
rhinitis groups is shown in Table 2. The
median eosinophil and basophilic
metachromatic cell scores in the rhini-tis
group were 1 and 2 whereas the
corresponding medians for the control
group, regardless of age, were both 0 (P
, .0001). None of the control sub-jects
had nasal eosinophil or basophilic
metachromatic cell scores more than 0.5.
Eosinophil scores and/or basophilic
metachromatic cell scores .0.5 were
therefore considered positive cut-off
points for the diagnosis of allergic rhi-
nitis. Sensitivities, specificities, posi-
tive predictive values, and negative
predictive values for various cut-offs
are shown in Table 3. Nasal basophilic
metachromatic cell scores .0.5 have a
better sensitivity as well as better neg-
ative predictive value than nasal eosin-
ophil scores .0.5. If one combines the
presence of eosinophil and basophilic
metachromatic cell scores .0.5 to be a
positive cut-off, the calculated sensi-
tivity, specificity, positive predictive
value, and negative predictive value
will be 54.17%, 100%, 100%, and
65.08%, respectively. Nevertheless, if
one considers only either eosinophil or
basophilic metachromatic cell scores
.0.5 as a cut-off, sensitivity, specific-
ity, positive predictive value and neg-
ative predictive value will improve to
91.67%, 100%, 100%, and 91.11%.
This cut-off provides the best diagnos-
tic utility.
In contrast, as shown in Table 4,
polymorphonuclear cell scores are not
good diagnostic indices for the pres-
ence of radiographic sinusitis. We
have tried using several cut-offs for
VOLUME 80, FEBRUARY, 2017
Number of Patient with BMC
Scores
Allergic Rhinitis Control
0 2 0 P 5 .12). Eosinophil scores, although
0 14 0 not statistically significant, increased
0 12 0 with age (r 5 0.16, P 5 .27) whereas
0 11 0
3 5 3
38 4 38
41 48 41
polymorphonuclear cell scores to de-
termine diagnostic significance of si-
nusitis and did not find any significant
correlation between polymorphonu-
clear cell scores and the presence of
radiographic sinusitis. This was per-
haps due to the presence of high num-
bers of polymorphonuclear cells in
healthy control children. In addition,
the likelihood ratio as defined by a
probability ratio between a disease and
non-disease group when the test is
pos-itive was calculated for varying
poly-morphonuclear cell scores. Tests
with better diagnostic value should
have likelihood ratio of either .10 or
,0.1.15 The results are tabulated in
Table 4. The likelihood ratio for poly-
morphonuclear cell scores 0.5 fell in
the 0.5 to 2 range indicating that this
parameter is a poor diagnostic test for
presence of sinusitis.
Correlations between the following
variables were calculated: symptom
and sign scores, symptom and cytol-
ogy scores, sign and cytology scores,
eosinophil and basophilic metachro-
matic cell scores, age and cytology
scores, age and diameters of skin tests
to Dermatophagoides pteronyssinus,
diameters of skin tests to Dermatopha-
goides pteronyssinus and cytology
scores. Symptom scores correlated
poorly with sign scores (r 5 0.11, P 5
.44) and cytology scores (eosinophils,
r 5 0.17, P 5 .25; basophilic meta-
chromatic cells, r 5 0.19, P 5 .20; and
polymorphonuclear cells, r 5 0.04, P 5
.78). In contrast, all categories of sign
scores correlated well with eosin-ophil
scores (r 5 0.38, P 5 .009) but
not with basophilic metachromatic cell
scores (r 5 0.26, P 5 .07) nor with
polymorphonuclear cell scores (r 5
0.008, P 5 .96). Eosinophil and baso-
philic metachromatic cell scores corre-
lated poorly to one another (r 5 0.22,
the basophilic metachromatic cell and
polymorphonuclear cell scores de-
creased with age (r 5 20.16 and 20.30,
P 5 .28 and .04 respectively).
Positive skin prick test results
among this group of children with al-
lergic rhinitis were as follows: Der-
matophagoides pteronyssinus 88.37%,
Dermatophagoides farinae 67.44%,
American cockroach 37.21%, shrimp
18.60%, soy 13.95%, crab 11.63%,
Johnson grass 11.63%, Bermuda grass
9.30%, Cladosporium 9.30%, egg
white 6.98%, cat 6.98%, Penicillium
6.98%, Aspergillus 6.98%, corn smut
6.98%, Alternaria 4.65%, mixed shell
fish 4.65%, Timothy grass 2.3%, Aca-
cia 2.3%, dog 2.3%, Fusarium 2.3%,
egg yolk 2.3%, beef 2.3%. Among
these children, 13.64% were sensitized
to single antigens, 22.73% to two an-
tigens, 13.64% to three antigens,
31.82% to four antigens, 9.09% to five
antigens and 2.27% were sensitized to
more than six antigens. Dermatopha-
goides pteronyssinus was the most
common antigen sensitized among
these allergic rhinitis children.
We further examined the relation-
ship between wheal sizes of Dermato-
phagoides pteronyssinus with age and
cytology scores. Wheal diameters to
Dermatophagoides pteronyssinus cor-
related poorly with both age (r 5
20.19, P 5 .35) and cytology scores
(eosinophil: r 5 0.25, P 5 .13, baso-
philic metachromatic cell: r 5 20.22, P
5 .19, polymorphonuclear cell: r 5
0.20, P 5 .23).
DISCUSSION
Our study indicated that nasal cytology
utilizing Rhinoprobes with Wright Gi-
emsa stain is a good diagnostic tool for
allergic rhinitis in children. The pres-
ence of either nasal eosinophil or ba-
sophilic metachromatic cell scores
167
Table 3. Sensitivity, Specificity, Positive Predictive Value (PPV) and Negative Predictive
Value (NPV) of Nasal Eosinophil (EOS) and Basophilic Metachromatic Cell (BMC) Score as a
Diagnostic Test for Allergic Rhinitis in Children
Test Sensitivity Specificity PPV NPV
EOS .0.5 64.58 100 100 70.69
BMC .0.5 81.25 100 100 82.00
EOS & BMC .0.5 54.17 100 100 65.08
EOS or BMC .0.5 91.67 100 100 91.11
Table 4. Sensitivity, Specificity, Positive Predictive Value (PPV) and Negative Predictive
Value (NPV) and Likelihood Ratio (LR) of Various Nasal Polymorphonuclear (PMN) Score as
a Diagnostic Test for Sinusitis in Children
Test Sensitivity Specificity PPV NPV LR
PMN $0.5 80.77 33.33 77.78 37.50 1.20
PMN $1 53.85 44.44 73.68 25.00 0.97
PMN $2 34.62 77.78 81.82 29.17 1.56
PMN $3 19.23 88.89 83.33 27.56 1.73
PMN $4 11.54 88.89 75.00 25.81 1.04
.0.5 provides the best sensitivity, nuclear cells are present in both nasal
specificity, positive predictive value, secretion and within the nasal mucosa.
and the best negative predictive value In contrast, basophilic metachromatic
for this condition. The distinction be- cells are found predominantly in the
tween control and allergic rhinitis nasal mucosa.13
groups using this cut-off could be Using mucosal scrapings with Han-
clearly observed in Table 2. None of sel's stain, Okuda et al reported that
the healthy children had eosinophil or most of the allergic patients had large
basophilic metachromatic cells with numbers of basophilic metachromatic
scores more than 0.5. This was con- cells (mean 505 6 830) comparing to 0
firmed by the results observed by Co- to 10 basophilic metachromatic cells in
hen et al that none of the healthy in- the majority of normal subjects.18 The
fants had nasal eosinophilia or only study in Thais was that by Jareon-
basophilia.16 charsri et al19 who studied adult and
Nasal cytology has been performed pediatric patients with ages ranged from
previously and reported using different 8 to 70 years old. In that study, nasal
specimen sources and different stain-ing scrapings stained with Hansel's stain
techniques. Miller et al determined the from patients with allergic rhini-tis
diagnostic value of eosinophils in nasal contained more basophilic meta-
secretion by Hansel's stain and found chromatic cells on their mucosal sur-
sensitivity and specificity for this faces than from nonallergic rhinitis and
method to be 70% and 94%, re- normal subjects, with a sensitivity of
spectively.11 Lee et al reported a eosi- 90.91%. The distinction of basophilic
nophil:neutrophil ratio in nasal secre- metachromatic cells from nasal epithe-
tions (by Wright-Giemsa stain) of $0.1 lium using Hansel's stain is quite dif-
to be a critical value for the dif- ficult in our experience. Nasal scraping
ferentiation between allergic and non- specimens obtained with Rhinoprobe
allergic nasal conditions.10 Comparing and stained with Wright-Giemsa stain, a
nasal biopsy specimens from patients method suggested by most investiga-tors
with symptomatic seasonal allergic in this field1,5 was therefore chosen for
rhinitis to a control group, Igarashi et al this study. With this method, the
demonstrated that nasal eosinophil distinction between eosinophils and
numbers were significantly higher in the basophilic metachromatic cells is quite
allergic group than in the control clear even to an inexperienced techni-
group.17 Eosinophils and polymorpho- cian. The test differentiates children
168 ANNALS OF ALLERGY, ASTHMA, & IMMUNOLOGY
with allergic rhinitis from normal chil-
dren with high sensitivity and specific-
ity (Table 3). This test can be utilized
as a screening tool prior to a consider-
ation of allergy skin testing. Further,
positive nasal cytology with negative
allergy skin testing establishes the di-
agnosis of nonallergic rhinitis with eo-
sinophilia (NARES),20 a condition
that is not commonly diagnosed
among children due to infrequent use
of nasal cytology in the diagnosis of
chronic rhinitis in this age group.
The presence of nasal polymorpho-
nuclear cells of any degree, on the other
hand, could be commonly found in
healthy children (Table 4). Our re-sults
confirm the findings of Cohen et al1 in
which 23% of normal children had
significant numbers of nasal poly-
morphonuclear cells.16 The presence of
polymorphonuclear cells in nasal spec-
imens, however, was found to be evi-
dence substantiating the diagnosis of
nasal infections, particularly sinusitis, in
some studies. Jong et al suggested that
the presence of polymorphonu-clear
cells of $5 per high power field by
Rhinoprobe correlated significantly with
radiographic sinusitis.12 The sen-sitivity
and specificity of polymorpho-nuclear
cells from that study were 100% and
53%, respectively. In our study,
polymorphonuclear cells corre-lated
poorly with radiographic appear-ance of
sinusitis and had poor sensitiv-ity for
this condition (Table 4). The likelihood
ratio also indicated that na-sal
polymorphonuclear cells have poor
diagnostic utility for sinusitis.
Symptom and sign scores among pa-
tients with allergic rhinitis correlated
poorly to each other. The reason for this
could be that most of our patients
suffered from longstanding nasal
blockages of perennial rhinitis and could
not differentiate varying degrees of nasal
blockages. A good correlation between
nasal eosinophil scores and sign scores
in our study substantiates findings by
Terada et al who demon-strated a
significant correlation be-tween the
increase in nasal airway re-sistance and
the number of activated nasal
eosinophils.21 In contrast, baso-philic
metachromatic cell scores in our
study did not correlate with symptom or
sign scores nor with eosinophil scores.
As basophilic metachromatic cells could
also be found in asymptom-atic siblings
of patients with allergic rhinitis (data not
shown), we postulate that basophilic
metachromatic cells are residential cells
that could be found in symptomatic as
well as in asymptom-atic allergic
rhinitis. The study of Wihl et al22 also
indicated that moderate numbers of
basophilic metachromatic cells could
still be seen even after the pollen season.
The natural history of eosinophils and
basophilic metachromatic cells in the
human nose is not well defined. Zeiger
et al studied high risk, atopic-prone
children and demonstrated that
prevalence and number of nasal baso-
philic metachromatic cells increased
from 4 months to 2 years of age and
remained at a plateau thereafter.5 Nasal
eosinophils, in contrast, increased from
4 months to 4 years without reaching a
plateau or a peak. Similarly, in our
study, we observed that basophilic
metachromatic cells decreased with age
whereas eosinophils increased with age,
although the relationship did not reach
statistical significance. Poly-
morphonuclear cells, on the other hand,
decreased with age.
In our study, Dermatophagoides
pteronyssinus was the most important
allergen these patients with allergic
rhinitis were sensitized to as has been
previously observed by our group. 23
Sensitization to grass pollens, the only
important seasonal outdoor allergen in
Thailand, is relatively low (less than
12%) among this group of children
which explains the perennial pattern that
is the most common form of rhi-nitis in
children in this country.24 It is prudent
to indicate that our findings may hold
true for children with peren-nial allergic
rhinitis until further results in those with
seasonal symptoms be-come available.
We could not identify any correlation
between wheal size of
Dermatophagoides pteronyssinus with
age nor with cytology scores. This was
perhaps due to several large positive of
skin tests to Dermatophagoides ptero-
nyssinus in young children.
VOLUME 80, FEBRUARY, 2017
In conclusion, eosinophil and baso-
philic metachromatic cells in nasal cy-
tology are a useful diagnostic test for
allergic rhinitis in children. Nasal eo-
sinophil and basophilic metachromatic
cells in children with allergic rhinitis
differed significantly from normal and
healthy children. Further, eosinophil
scores correlated well with signs of
allergic rhinitis in children.
ACKNOWLEDGMENT
The authors thank Harold S Nelson,
MD for his kind revision and sugges-
tions in preparing the manuscript.
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ANNALS OF ALLERGY, ASTHMA, & IMMUNOLOGY
Accepted for publication. J Med
Assoc Thai 1997.
Request for reprints should be addressed to:
Pakit Vichyanond, MD
Division of Allergy & Immunology
Department of Pediatrics
Siriraj Hospital, Mahidol University
Bangkok 10700
Thailand