Allergic Rhinitis Diagnosis Skin-Prick Test Versus

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262 Original article

Allergic rhinitis diagnosis: skin-prick test versus laboratory


diagnostic methods
Hany S. Mostafaa, Mohamed Qotba, Mohammed A. Husseina,
Ahmed Husseinb
a
Department of ENT, Fayoum University, Aim
Fayoum, bDepartment of ENT, Cairo University, To verify the specificity, sensitivity, and accuracy of the skin-prick tests (SPTs) in
Cairo, Egypt
allergic rhinitis (AR) compared with blood tests and nasal smears.
Correspondence to Hany S . Mostafa, MSc, Study design
MD, Karma 2, 15643, Egypt.
It is a cohort, prospective, nonrandomized study.
e-mail: hanysam2002@yahoo.com
Patients and methods
Received 10 September 2018 A total of 180 patients were enrolled. Group A included 135 patients having AR
Accepted 21 December 2018
symptoms for more than 1 year. Group B included 45 patients without AR symptoms
The Egyptian Journal of Otolaryngology candidate for septoplasty surgery who served as controls. All patients were
2019, 35:262–268 subjected to detailed history, scoring for AR, endoscopic examination, complete
blood count, nasal smear eosinophilia, and SPT.
Results
SPT was positive in 94.1% (n=127) of allergic patients and 20% (n=9) of the
controls at least for one allergen. Most of cases were allergic to mixed pollens
(66.7%), cotton dust (41.5%), and housefly particles and house dust mite (28.9%
equally). The absolute eosinophil count was positive in 70.4% of allergic patients
(n=95) and 33.3% of the control (n=15). Nasal smear eosinophilia was positive in
82.9% (n=112) of allergic patients and 20% (n=9) of the controls. SPT possesses
high sensitivity and specificity that reached 94.1 and 80%, respectively, and 90.6%
accuracy. However, absolute eosinophil count showed the lowest results, where
sensitivity and specificity reached 70.4 and 66.7%, respectively, and 69.4%
accuracy.
Conclusion
SPT is accurate for diagnosing AR and possesses high sensitivity and specificity;
however, adding a nasal swap test will raise the sensitivity, specificity, and accuracy
of diagnosis.

Keywords:
absolute eosinophilic count, allergic rhinitis, nasal smear eosinophilia, skin-prick test
Egypt J Otolaryngol 35:262–268
© 2019 The Egyptian Journal of Otolaryngology
1012-5574

of patients and their response to medical treatment [5].


Introduction
Proof of sensitization to an allergen includes coupling
Allergic rhinitis (AR) is a global health problem and
of skin or blood testing and patient’s exposure history
one of the most common disorder seen by
[6].
otolaryngologists, the prevalence rate of AR had
been reported as 10–30% of adults and up to 40% of
Skin-prick testing (SPT) is advised as a diagnostic tool
children [1]. AR is an immunoglobulin E (IgE)-
for AR as it is less invasive and easy to administer [7].
mediated disease, which is predominantly caused by
When SPT result is negative, AR as an IgE-mediated
environmental allergen exposure in a genetically
disease is largely excluded. Moreover, the results of
predisposed individual. Common allergens
SPT are important, especially if avoidance measures or
implicated in AR are mainly proteins and
immunotherapy are to be considered. There is a lack of
glycoproteins found in airborne particles. Important
international consensus regarding the accuracy of skin
allergens causing intermittent or persistent symptoms
testing in the diagnosis of allergies [8,9], including AR
may be airborne dust mite, cockroach residues, animal
[10,11]. The disagreement in the precision of SPT in
dander, and grass pollens [2].
the diagnosis of AR among studies can be clarified by
AR is characterized by the presence of nasal
obstruction, congestion, rhinorrhea with or without This is an open access journal, and articles are distributed under the terms
of the Creative Commons Attribution-NonCommercial-ShareAlike 4.0
facial pain, and reduction or loss of smell [3,4]. These License, which allows others to remix, tweak, and build upon the work
symptoms are reversible either spontaneously or with non-commercially, as long as appropriate credit is given and the new
treatment. AR is diagnosed by the clinical examination creations are licensed under the identical terms.

© 2019 The Egyptian Journal of Otolaryngology | Published by Wolters Kluwer - Medknow DOI: 10.4103/ejo.ejo_8_19
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Allergic rhinitis diagnosis Mostafa et al. 263

the inconsistency of standardization in the composition patients attending otorhinolaryngology outpatient


of allergens, the device used in the test, the differences clinic of Fayoum University Hospital, during the
in the characteristics of tested population, or the design period from September 2016 to September 2018.
of the study [12]. This study was approved by local ethical committee.
Written consents were provided by all the patients.
When SPT is not available, or the patient is receiving
antihistamines, other tests should be considered Patients are scored according to the quantitative
including: complete blood picture to detect absolute scoring for allergic rhinitis (SFAR) [19]. Patients
eosinophil count (AEC), total and allergen-specific with SFAR score of more than or equal to 7 are
IgE concentrations in the blood, and nasal smears considered to have AR, whereas patients with SFAR
for cytology, which may show high concentrations of score of less than 7 are considered to have no AR.
eosinophils [13]. SPT has the following advantages
when compared with an in-vitro measurement of Patients were divided into two groups: group A
specific IgE antibodies: it can be interpreted within included 135 patients presented with AR symptoms
15–20 min versus in-vitro test results (days or weeks); it for more than 1 year and had SFAR score of more than
can also be used to test less common allergens that lack or equal to 7; they served as AR patients. Group B
specific IgE antibody measurements, such as fresh included 45 patients candidate for septoplasty surgery
fruits and vegetables, and certain medications; the without evidence of previous history of AR with SFAR
test gives a visual indication of the sensitivity which score of less than 7; they served as control patients.
can be used to affect the patient’s behavior [14]; it is less Both groups did have similar criteria regarding no
expensive; and it is a more specific screening method medical treatment either oral, topical corticosteroids,
for detecting the presence of IgE antibodies in patients or oral antihistamines at least 4 weeks before the first
who had appropriate exposure history [15]. visit. Patients with severe dermatographism, patients
on beta-blockers, uncooperative patients, those unable
The commercially available respiratory allergens have to stop antihistamines, pregnant patients, patients with
few systemic adverse effects; however, a physician or severe asthma, patients with drug-induced rhinitis, or
other health care professional and emergency those with cardiac disease, with contraindication to the
equipment should be immediately available when use of epinephrine, were excluded from the present
such tests are performed, and in patients with a study. All patients were subjected to detailed history,
history of severe systemic allergic reactions to food endoscopic examination, complete blood count (CBC),
or drugs, an intravenous line for immediate circulatory nasal smear eosinophilia (NSE), and SPT.
access can be recommended. Patients, especially those
taking a beta blocker, or less often, angiotensin Skin-prick test
converting enzyme-inhibitor, may be at a higher risk SPT was done by introducing specific allergens like
because of less response to epinephrine that might be house dust, house dust mite, cotton dust, mixed
needed to treat a systemic allergic reaction [16]. pollens, mixed molds, housefly particles, and grass
pollens into the volar part of the forearm of patient’s
Relative contraindications for SPT include pregnancy skin. The test solutions were allergen extracts (in 50%
[17], a peak flow of less than 70% in patients with glycerine), one negative control (nonextract containing
asthma, patients with dermographism and severe diluent with 50% glycerine), and one positive control
eczema, or patients who are taking medications such (histamine base 6 mg/ml) purchased from Greer
as antihistamines or antidepressants or calcineurin Laboratories Inc. (Lenoir, North Carolina, USA).
inhibitors, which can interfere with the proper
interpretation of the test results [18]. The process of skin inoculation with allergens was done
using a single-head metal lancet (ALK-Abello Inc.,
The current study is implemented with the aim to Horshlom, Denmark) (Fig. 1).
verify the specificity, sensitivity, and accuracy of SPT
compared with inexpensive laboratory tests and nasal Positive and negative controls were measured first. The
smears in the diagnosis of AR. (positive) histamine control was used to make sure that
the test materials are applied correctly and to exclude
negative SPT results owing to medications taken by the
Patients and methods test participant. The negative control excludes the
The current study is a cohort, prospective, presence of dermographism, which, when present,
nonrandomized study. Data were collected from makes the tests difficult to interpret. The largest
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264 The Egyptian Journal of Otolaryngology, Vol. 35 No. 3, July-September 2019

Figure 1 Figure 2

The process of skin inoculation with different allergens using a single- The result of SP after 15 min.
head metal lancet (ALK-Abello Inc.).

diameter of the wheal of each particular test is Table 1 Self-completed questionnaire for the scoring for
allergic rhinitis [19]
measured. A positive result being a wheal of more
than or equal to 3 mm. Then the wheal is outlined Items Score Total
(points) score
with a pen blotted onto a cellophane tape and
Nasal symptoms (blocked nose, runny 1 for each 3
transcribed onto paper and stored electronically, as nose, and sneezing) in past year symptom
recommended by the American Academy of Allergy, 1 for 4
Asthma and Immunology, and the American College perennial
of Allergy, Asthma, and Immunology [7] (Fig. 2 and 1 for pollen 5
season
Table 1).
Nasal symptoms plus itchy-watery eyes 2 7
Triggers
CBC was performed to detect AEC, which refers to Pollens, house dust mites, and dust 1
the number of circulating eosinophils in the peripheral Epithelia (cat and dog) 1 9
blood in cells per cubic millimeter (cells/mm3). The Previous allergic status 2 11
cutoff value used in this study was positive if AEC was Previous positive allergic tests 2 13
more than or equal to 440 cells/mm3 [20]. Previous medical diagnosis of allergy 1 14
Familial history of allergy 2 16

Nasal smear was taken by swab sticks from medial


surface of middle part of inferior turbinate. The slide number and percentages. Sensitivity, specificity, and
was fixed in 95% ethyl alcohol, and then stained with total accuracy measures of different tests in
hematoxylin and eosin stain. Finally, the slide was differentiating patients of AR from normal were
subjected to NSE count study. The cutoff value used presented as %, with 95% confidence interval, and
in this study was positive if more than or equal to 10 calculated using OpenEpi (Open Source
eosinophil cells were detected by high power field (E Epidemiologic Statistics for Public Health, Developed
≥10/HPF) [21]. by the open Epi project, Atlanta, Georgia) version 3.01.

The collected data were organized, tabulated, and


statistically analyzed using SPSS software statistical Results
computer package, version 18 (SPSS Inc., Chicago, This study was carried out on 180 patients, who were
Illinois, USA). Qualitative data were presented as divided into two groups. Group A included 135
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Allergic rhinitis diagnosis Mostafa et al. 265

patients having AR and group B included 45 cases who The sensitivity, specificity, and accuracy among the
served as the control. The first group (group A) had 92 three types of tests are summarized in Table 6. SPT
males and 43 females, with an average age of 25.2 years, possess the highest result, as sensitivity and specificity
whereas the control group (group B) had 34 males and reached 94.1 and 80%, respectively, and 90.6%
11 females, with an average age of 25.4 years (Table 2). accuracy. On the contrary, AEC showed the
lowest results, where sensitivity and specificity
Overall, 60% of patients with AR (n=81) had severe reached 70.4 and 66.7%, respectively, and 69.4%
allergic symptoms that affected their daily life whereas accuracy (Fig. 4).
only 5.9% of patients (n=8) had mild symptoms. None
of the control group had any allergic symptoms.
Discussion
Regarding the SPT, 94.1% of allergic patients (n=127) AR can be defined clinically as an inflammatory
showed positivity at least for one allergen, whereas condition of the nose characterized by nasal
5.9% of them (n=8) showed no reaction to any allergen obstruction, sneezing, itching, or rhinorrhoea [13].
but had positive eosinophil nasal smears. On the A recent large-scale, cross-sectional study in six
contrary, 20% of the control group (n=9) showed western European countries found that the overall
skin reaction to at least one allergen, with maximum prevalence of AR was 23%. The study also showed
of three allergens (Table 3). that the condition is often undiagnosed, as 45% of
patients with investigator-confirmed AR had not
Most of cases were allergic to mixed pollens (66.7%), previously received a diagnosis from their physicians
cotton dust (41.5%), and housefly particles and house [22].
dust mite equally (28.9%). In many patients there was
reaction to multiple allergens. Most of the control Since the first publication about SPT by Ebruster [23],
group participants were allergic to mixed pollen also who extensively researched this diagnostic test, it has
(6.75%) and grass and house dust mite equally at 4.4% been used as a primary diagnostic tool to detect type I
(Fig. 3). hypersensitivity reactions. Although the principle of
SPT still largely resembles the original methods
The AEC in the allergic patients was positive (>440 described, a wide array of interpretations and
cell/mm3) in 70.4% of them (n=95), whereas it was modifications has led to diminished comparability
negative (<440 cell/mm3) in 29.6% (n=40). In the when SPT results are reported [24].
control group, only 33.3% of patients (n=15) were
positive (Table 4). Adopting the Global Allergy and Asthma European
Network (GA (2) LEN) protocol, Heinzerling et al.
Regarding the NSE count, in the AR group, 82.9% of [14] found SPT is highly specific and sensitive,
patients (n=112) had positive nasal smear results (<10 reaching 70–95% and 80–97%, respectively, to
eosinophils/HPF), whereas 17.1% of patients (n=23) diagnose inhalant allergies. The positive predictive
had negative results (>10 eosinophils/HPF). In the value to diagnose AR based only on the clinical
control group, 20% of patients (n=9) were positive history is 77% for persistent allergy and 82–85% for
(Table 5). intermittent seasonal allergy, this increases to 97–99%
if SPT is utilized [25].
Table 2 The demographic data
Group A Group B It was reported in a meta-analysis done by Nevis et al.
[26] to verify the sensitivity and specificity of SPT in
No 135 45
M 92 34
the diagnosis of AR that there is a lack of consensus
F 43 11 regarding the performance of SPT, and the combined
Average age 25.2 25.4 estimates of the sensitivity and specificity for SPT in
various studies were 88.4 and 77.1%, respectively.
Table 3 A comparison between skin-prick test among allergic
rhinitis and control groups When we compare the results reached in the present
SPT Group A (cases) [n (%)] Group B (control) [n (%)] study with the aforementioned meta-analysis, it
Positive 127 (94.1) 9 (20) showed great concordance, as in the current study,
Negative 8 (5.9) 36 (80) SPT is reasonably accurate reaching 90.6% in
Total 135 (100) 45 (100) identifying patients with suspected symptoms of AR.
SPT, skin-prick test. It carries sensitivity and specificity of 94.1 and 80%,
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266 The Egyptian Journal of Otolaryngology, Vol. 35 No. 3, July-September 2019

Figure 3

Results of the SPT among AR cases and controls for different allergens (%). AR, allergic rhinitis; SPT, skin-prick test.

Table 4 A comparison between absolute eosinophil count Table 6 Results of sensitivity, specificity, and accuracy
results among allergic rhinitis and control groups among the three types of tests
Group A [n (%)] Group B [n (%)] Sensitivity (95% Specificity (95% Accuracy (95%
CI) CI) CI)
>440 cell/mm 3
95 (70.4) 15 (33.3)
<440 cell/mm3 40 (29.6) 30 (66.7) SPT 94.1 (88.7–96.9) 80.0 (66.2–89.1) 90.6 (85.4–94.2)
Total 135 (100) 45 (100) NSE 82.9 (75.7–88.4) 80.0 (66.2–89.1) 82.2 (75.9–87.1)
AEC 70.4 (62.2–77.4) 66.7 (52.1–78.6) 69.4 (62.4–75.7)
AEC, absolute eosinophil count; CI, confidence interval; NSE,
Table 5 Comparison of percentage of eosinophils in nasal nasal smear eosinophilia; SPT, skin-prick test.
smears among allergic rhinitis and control groups
Group A [n (%)] Group B [n (%)] It is well known that the proper diagnosis of allergen in
E≤10/HPF 112 (82.9) 9 (20) patients with AR will facilitate the decision of further
E< 10/HPF 23 (17.1) 36 (80) management of patients in the form of
Total 135 (100) 45 (100) immunotherapy, allergen avoidance, or
pharmacotherapy. Consequently, financial burden
respectively. On the contrary, nasal smears had can be alleviated and the patients’ quality of life can
sensitivity and specificity of 82.9 and 80%, be improved. This raises the importance of SPT
respectively, whereas AEC had sensitivity and compared with serum eosinophilia and nasal swab,
specificity of 70.4 and 66.7%, respectively, which are as the SPT can diagnose the AR in addition to
lower than SPT. suspected allergen. On the contrary, CBC (AEC)
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Allergic rhinitis diagnosis Mostafa et al. 267

Figure 4

Sensitivity, specificity, and accuracy of SPT, AEC, and NSE. AEC, absolute eosinophil count; NSE, nasal smear eosinophilia; SPT, skin-prick
test.

and nasal smear (NSE) only detect AR without AR. SPT should be further standardized to include
detection of allergen, but adding CBC (AEC) and standardized procedures and allergen panels that
nasal smear (NSE) to SPT will increase the accuracy, cover suspected allergens in different geographic
sensitivity, and specificity of diagnosis in AR. areas.

The current study can add to the results of several Financial support and sponsorship
studies that support the role of SPT as an accurate test Nil.
in the diagnosis of AR. The present study was done on
a small number of patients, and further studies are Conflicts of interest
needed on large numbers of patients to evaluate the role There are no conflicts of interest.
of SPT, CBC (AEC), and nasal smear (NSE) in the
diagnosis of AR.
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