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Systematic & Applied Acarology 23(2): 206–215 (2018)
http://doi.org/10.11158/saa.23.2.2 ISSN 1362-1971 (print)
ISSN 2056-6069 (online)
206
© Systematic & Applied Acarology Society
Article
Evaluation of Dermatophagoides pteronyssinus (Trouessart) and D. farinae
Hughes (Acari: Pyroglyphidae) sensitivity in patients with allergic rhinitis: a
comparative study
ERHAN EYTUN
1*
, SAL H DO AN
1
, EDHEM ÜNVER
2
& FAT H ÖZÇ ÇEK
3
1
Department of Biology, Arts & Sciences Faculty, Erzincan University, Erzincan, Turkey
2
Department of Chest Disease, Erzincan University School of Medicine, Erzincan, Turkey
3
Department of Internal Medicine, Erzincan University School of Medicine, Erzincan, Turkey
* Corresponding author: ezeytun@erzincan.edu.tr
Abstract
This study was conducted to determine the sensitivity to Dermatophagoides pteronyssinus (Trouessart) and D.
farinae Hughes with skin prick tests (SPT) and serologic tests in patients with allergic rhinitis (AR), and to
specifically search for those mites in homes of patients. A total of 51 participants, (23 patients and 28 controls)
were utilized. Skin-prick tests with D. pteronyssinus and D. farinae allergens were performed on all participants,
and serum levels of allergen-specific lgE and total IgE were also measured. Dust samples were collected from
homes of all participants and examined under a stereo microscope. 977 D. pteronyssinus (mean 44.4/g) and 24
D. farinae (mean 4.0/g) were isolated from the homes of patients, whereas 35 D. pteronyssinus (mean 4.4/g),
and four D. farinae (mean 2.0/g) were isolated from the homes of the controls. Patients with D. pteronyssinus
in their homes had 95.5% sensitivity to the species according to SPT and 27.3 according to IgE. Patients with
D. farinae in their homes had 83.3% sensitivity to the species according to SPT, and 50% according to IgE.
Dermatophagoides pteronyssinus sensitivity in the controls was detected as 12.5% according to SPT; however,
D. farinae sensitivity was not detected according to both SPT and mite-specific IgE. Differences between
patients and controls utilizing SPT results was statistically significant, but not when using mite-specific IgE
results. As a result, it was determined that patients with AR in Erzincan province were sensitized to D.
pteronyssinus and D. farinae, and that their homes contained those species. It may be helpful to consider these
findings in clinical assessment of patients with AR, and also in treatment utilizing immunotherapy techniques.
Keywords: Allergic rhinitis, allergens, Dermatophagoides, house dust mite, immunotherapy
Introduction
House dust mites (HDMs) are microscopic arthropods belonging to the class Arachnida, superorder
Acariformes (Zhang et al. 2011). The term “house dust mite” is usually used for Dermatophagoides
pteronyssinus (Trouessart), D. farinae Hughes, and Euroglyphus maynei (Cooreman) living in house
dust and belonging to the family Pyroglyphidae (Spieksma 1997; Colloff 2009; Aykut et al. 2013a,
2016; Zeytun et al. 2017). The main biotopes of HDMs are mattresses, pillows, carpets, fabric-
covered furniture, velvet curtains, and fuzzy toys (Somorin et al. 1978; Colloff 2009). The primary
nutritional sources for mites are skin scales rich in proteins and lipids and the microorganisms living
on skin (Colloff 2009). They are known to play a role in etiology of some allergic diseases, namely
allergic asthma, allergic rhinitis, allergic conjunctivitis, and atopic dermatitis (Bousquet et al. 2008;
Colloff 2009).
Allergic rhinitis (AR) is an upper respiratory tract disease that develops through specific IgE as
a result of exposure of the nasal mucosa to allergens (Bousquet et al. 2008). Although not fatal, this
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ZEYTUN ET AL.: SENSITIVITY TO HDMS IN PATIENTS WITH ALLERGIC RHINITIS
disease decreases quality of life, causes considerable loss of schooling and working, and is a burden
to the community both socially and economically. Its prevalence varies from country to country
depending on the respiratory-allergen load. Allergens include plant pollens, fungi, occupational
allergens, and HDMs. The most common and effective HDM allergens are Der p, from D.
pteronyssinus exposure and Der f, from D. farinae exposure. The allergenic features of HDMs are
caused by their feces and their body tissues (Colloff 2009; Calderon et al. 2015; Vidal-Quist et al.
2015). Over time, mite feces and body-tissue residues from their fragmentation after death
accumulate in carpets, fabric-covered furniture, fuzzy toys, mattresses, and pillows. These allergens
remaining suspend in air for a time and mix with air taken into the respiratory track, thereby
stimulating immune-system elements (Bousquet et al. 2008).
Many studies have been performed worldwide on the distribution and determination of HDM
species, allergen types and levels, and their relationship to several allergic diseases. In a previous
study, Zeytun et al. (2017) investigated the sensitivity to HDMs in allergic asthmatic patients;
however, to the best of our knowledge, there are no studies that specifically searched for mites in the
homes of patients with AR and also evaluated skin and serologic test outcomes. The present study
was conducted to determine the sensitivity to D. pteronyssinus and D. farinae utilizing skin and
serologic tests in patients with AR, and to search for mites in their homes. Such studies are important
for a better understanding of the role HDMs play in the allergic rhinitis etiology.
Material and Method
Invstigations were conducted between January 2014 and June 2014 in Erzincan, Turkey, a province
that has approximately 100,000 inhabitants, an elevation of 1,185m above sea level, and a
continental climate. The study group included 23 patients examined at the Clinics of Otolaryngology
and Chest Diseases at the Mengücek Gazi Training and Research Hospital and diagnosed with AR
according to ARIA (Allergic Rhinitis and its Impact on Asthma) criteria (Bousquet et al 2008).
Twenty-eight healthy people without allergic rhinitis symptoms such as sneezing, watery
rhinorrhoea, nasal obstruction, itching of nose and throat, and ear and eye symptoms (e.g. in the form
of redness, watering and itching) in the clinical examination were selected as the control group. The
study was approved by the Erzincan University Ethics Committee (Decision : 2014-02/06), and
all participants signed informed consent forms prepared in accordance with the Helsinki Declaration.
All participants were subjected to skin prick tests for the determination of sensitivity to D.
pteronyssinus and D. farinae, and their serum levels for allergen-specific lgE and total IgE were
measured. Der p and Der f solutions (Lofarma; Milano, Italy) were used as the HDM allergens in the
SPT, and the evaluation was done after 15 minutes. Indurations of 3 mm or greater were considered
positive. Levels of allergen-specific IgE were measured with the immunoblot method, while the total
IgE level was determined by the CLIA (Chemi Luminescence Immuno Assay) method. Specific IgE
levels of 0.35 kUA/L and total IgE values of 87 U/mL were considered positive.
Methods for the collection of dust samples, and the extraction, preparation and identification of
mite specimens follow the method used by Zeytun et al. (2016, 2017).
Data were analyzed using SPSS 20.0 (Statistical Package for Social Sciences; Chicago, IL,
USA). The Kolmogorov–Smirnov test was used to check for normal distribution of variables. A
Mann-Whitney U-test was used to compare non-normally distributed variables between the groups.
Pearson correlation test was used to correlate mite density and IgE levels. The chi-square test was
used to compare categorical data. A probability value of 0.05 or less was considered statistically
significant.
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SYSTEMATIC & APPLIED ACAROLOGY VOL. 23
Results
Twenty-three patients (median age 32, min. age 16, max. age 60; 17 females and six males) and 28
controls (median age 25, min. age 17, max. age 69; 10 females and 18 males) were included in the
study (Table 1).
TABLE 1. Demographic characteristics of the patients and controls.
min: minimum, max: maximum
a
Mann Whitney-U test
b
Chi square test
Dermatophagoides pteronyssinus positivity of patients and controls was detected as 91.3% and
39.3% respectively, according to the SPT results, and the differences between groups was found
statistically significant (p<0.001). Dermatophagoides farinae positivity was found in 43.5% of
patients and 25% of controls, but no significant difference was found between the groups. According
to the mite-specific IgE results, 30.4% of patients had D. pteronyssinus-specific IgE positivity
(p=0.002), and 34.8% had D. farinae-specific IgE positivity (p=0.001), while all the controls were
negative. The level of total IgE were high in 39.1% of patients and 10.7% of controls (p=0.017)
(Table 2).
TABLE 2. The results of serologic and skin prick test of patients and controls.
SPT: Skin prick test
a
Chi square test
b
Mann Whitney-U test
Comparison using the microscopic examination data, specific-mite positivity of homes of the
patients and the controls were detected as 100% and 35.7% respectively, and differences were found
to be statistically significant (p<0.001). Overall, 1001 mites were isolated from homes of the patients
(977 (mean 44.4/g) D. pteronyssinus (Figures 1-2) and 24 (mean 4.0/g) D. farinae (Figures 3-4)),
Patients Controls P value
Age (Years)
Median (min – max)] 32 (16–60) 25 (17–69) >0.05
a
Sex
Female
Male 17 (73.9%)
6 (26.1%) 10 (35.7%)
18 (64.3%)
<0.05
b
Patients Controls P value
SPT positivity
D. pteronyssinus 21/23 (91.3%) 11/28 (39.3%) <0.001
a
D. farinae 10/23 (43.5%) 7/28 (25%) 0.164
a
Specific IgE positivity
D. pteronyssinus 7/23 (30.4%) 0/28 (0%) 0.002
a
D. farinae 8/23 (34.8%) 0/28 (0%) 0.001
a
Total IgE level
Normal ( 87 U/mL) 14/23 (60.9%) 25/28 (89.3%) 0.017
a
High ( 87 U/mL) 9/23 (39.1%) 3/28 (10.7%)
Mean (min-max) 254.1 (1-1400) 51.4 (1.5-310) 0.048
b
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ZEYTUN ET AL.: SENSITIVITY TO HDMS IN PATIENTS WITH ALLERGIC RHINITIS
and 39 from homes of the controls (35 D. pteronyssinus (mean 4.4/g), four D. farinae (mean 2.0/g)).
A statistically significant difference was found between the homes of patients and controls in regard
to D. pteronyssinus positivity and density (p<0.001), but a significant difference not found with
regard to D. farinae positivity and density (p>0.05) (Table 3).
FIGURE 1. Dermatophagoides pteronyssinus (female).
FIGURE 2. Dermatophagoides pteronyssinus (male).
On the other hand, when SPT and serolgic test results were compared with the presence of mites
in the homes, D. pteronyssinus sensitivity of patients with D. pteronyssinus in their homes were
detected as 95.5% according to SPT, and 27.3 according to IgE. Dermatophagoides farinae
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SYSTEMATIC & APPLIED ACAROLOGY VOL. 23
sensitivity of patients with D. farinae in their homes was detected as 83.3% according to SPT, and
50% according to IgE. Dermatophagoides pteronyssinus sensitivity in the controls were detected as
12.5% according to SPT, but D. farinae sensitivity was not detected, according to both SPT and mite-
specific IgE results. Differences between patients and controls according to SPT results was
statistically significant, but not significant according to mite-specific IgE results. Both D.
pteronyssinus and D. farinae sensitivity of patients who had presence of both mite species in their
homes were detected as 80% according to SPT, and 40% according to IgE. But there were no controls
who was be sensitive to both D. pteronyssinus and D. farinae. In addition there were no controls who
had presence of both D. pteronyssinus and D. farinae in their homes. Differences between patients
and controls according to both SPT and mite-specific IgE results was statistically significant (Table
4). In addition, a positive correlation between mite density in homes of patients and serum IgE and
total IgE levels was found (r: 0.751 and r: 0.526 respectively), while not found in controls (r: -0.208
and r: -0.188 respectively) (Table 5).
TABLE 3. The presence and density of mites in homes of patients and controls
.
a
For the calculation of the number of mean mite (dust/g) only the mite positive homes have been taken into account's.
b
Chi square test
c
Mann Whitney-U test
Discussion
Numerous studies to evaluate HDM sensitivity in allergic patients have been undertaken. Those
studies report that D. pteronyssinus and D. farinae positivity in patients with AR, according to SPT
results, as follows: 82% and 82%, respectively in Malaysia (Ho et al. 1995); 76% and 79% in
Thailand (Pumhirun et al. 1997); 80% and 79%, in Chile (Calvo et al. 2005); 50.8% and 47.9% in
Omani (Al-Tamemi et al. 2008); 92% and 68% in South Africa (Seedat et al. 2010); 80.3% and
83.7% in China (Zhang et al. 2012) and 90.1% and 90.8% in Venezuela (Sanchez-Borges et al.
2014). Studies in Turkey have reported these rates as 62.2% and 51.3% respectively in Eski ehir
(Harmancı et al. 2000); 72.5% and 63.7% in Düzce (Öztürk et al. 2005); and 22.4% and 21.5% in
Isparta (Yasan et al. 2006). Results of all these studies show that D. pteronyssinus positivity,
according to SPT results, varied between 22.4% and 92%, and that D. farinae positivity varied
Homes of Patients Homes of Controls P value
Total (specific-mite)
Mite positive 23/23 (100%) 10/28 (35.7%) <0.001
b
a
Mean mite (dust/g) 43.5 3.9 <0.001
c
a
Total mite (dust/g) 1001 39
D. pteronyssinus
Mite positive 22/23 (95.7%) 8/28 (28.6%) <0.001
b
a
Mean mite (dust/g) 44.4 4.4 <0.001
c
a
Total mite (dust/g) 977 35
D. farinae
Mite positive 6/23 (26.1%) 2/28 (7.1%) 0.064
b
a
Mean mite (dust/g) 4.0 2.0 0.068
c
a
Total mite (dust/g) 24 4
2112018
ZEYTUN ET AL.: SENSITIVITY TO HDMS IN PATIENTS WITH ALLERGIC RHINITIS
between 21.5% and 90.8%. Our results are in agreement with those ranges: D. pteronyssinus and D.
farinae SPT positivity in patients was 91.3% and 43.5% respectively.
TABLE 4. Sensitivity to Dermatophagoides pteronyssinus and D. farinae in patients and controls according to
skin and serological test results.
SPT: Skin prick test
a
Participants only who had presence of D. pteronyssinus in their home have been taken into account's.
b
Participants only who had presence of D. farinae in their home have been taken into account's.
c
Participants only who had presence of both D. pteronyssinus and D. farinae in their home have been taken into account's
d
Chi square test
FIGURE 3. Dermatophagoides farinae (female).
In other studies D. pteronyssinus and D. farinae-specific IgE positivity in AR patients have been
reported as 37% and 34% in USA (Chew et al. 2009); 61.1% and 60.2% in China (Zhang et al. 2012);
72% and 80% in Philippines (Valmonte et al. 2012); and 51.6% and 52.2% respectively in Korea
(Kim et al. 2015). Studies in Turkey have reported these rates as 79% and 85%, respectively, in
Eski ehir and 27.5% and 17.5% in Afyon (Harmancı et al. 2000; Çiftçi et al. 2004). These studies
show that D. pteronyssinus-specific IgE positivity varies between 27.5% and 79%, while D. farinae-
Patients Controls P value
d
a
Sensitivity to D. pteronyssinus
According to SPT result 21/22 (95.5%) 1/8 (12.5%) <0.001
According to mite-specific IgE result 6/22 (27.3%) 0/8 (0%) 0.099
b
Sensitivity to D. farinae
According to SPT result 5/6 (83.3%) 0/2 (0%) 0.035
According to mite-specific IgE result 3/6 (50%) 0/2 (0%) 0.206
c
Sensitivity to both D. pteronyssinus and D. farinae
According to SPT result 4/5 (80%) 0/0 (0%) 0.001
According to mite-specific IgE result 2/5 (40%) 0/0 (0%) 0.002
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SYSTEMATIC & APPLIED ACAROLOGY VOL. 23
specific IgE positivity varies between 17.5% and 85%. In the present study, however, D.
pteronyssinus positivity in patients, according to mite-specific IgE results, was 30.4%, and D.
farinae positivity was 34.8%, while all the controls were found to be negative for both mites. Our
findings are consistent with the literature; however, there are differences in the percentage ranges
among the studies that may be a result of the degree of the patients’ sensitization or to differences in
the study methods. On the other hand, another method used to support clinical findings in the
diagnosis of AR is the determination of serum total IgE level. Bousquet et al. (2008) have reported
elevated total IgE levels in allergic and parasitic diseases. In our study, serum levels of total IgE were
detected higher in 39.1% of patients and 10.7% of the controls. Similarly, other studies have reported
that levels of total IgE was high in patients with AR (Akkaya et al. 1995; Vartiainen et al. 2002;
Öztürk et al. 2005; Yasan et al. 2006; Yılmaz et al. 2009).
TABLE 5. The correlation between mite density and IgE levels
.
r: correlation coefficient; min: minimum; max: maximum
a
Pearson correlation test
FIGURE 4. Dermatophagoides farinae (male).
To date, numerous faunistic studies have been conducted on HDMs that are thought to play a
role in the pathogenesis of several diseases, including AR, allergic asthma, allergic dermatitis, and
allergic conjunctivitis. The prevalence of D. pteronyssinus and D. farinae in homes of patients with
AR was reported as 98.2% and 5.5% in La Coruna, 98.8% and 4.8% in Lugo, 93.3% and 6.7% in
Patients P value
a
(r) Controls P value
a
(r)
Mite density (dust/g)
Median (min – max)
7
(1–628) < 0.001
(0.751)
0
(0–8) 0.287
(-0.208)
Specific IgE levels (kUA/L)
Median (min – max)
0.20
(0.05–3.90)
0.10
(0.05–0.030)
Mite density (dust/g)
Median (min – max)
7
(1–628) 0.010
(0.526)
0
(0–8) 0.338
(-0.188)
Total IgE levels (U/mL)
Median (min – max)
58.2
(7.1–1400)
19.7
(1.5–310)
2132018
ZEYTUN ET AL.: SENSITIVITY TO HDMS IN PATIENTS WITH ALLERGIC RHINITIS
Ourense, 100% and 2.2% in Pontevedra, and 31.8% and 35.6% in Murcia, Spain, and 40% and 20%,
in Nigeria (Somorin et al. 1978; Boquete et al. 2006; Pagan et al. 2012). Studies in Turkey reported
that prevalence of D. pteronyssinus in the homes of patients with AR was 27.5% in Afyon, 46.3% in
Malatya, and 18.8% in Kütahya, but D. farinae not detected (Çiftçi et al. 2004; Atambay et al. 2006;
Akdemir & Yılmaz 2009). However, in other faunistic studies conducted in Turkey in the homes of
individuals who did not have AR or any other illness, prevalence of D. farinae varied between 0.2%
and 15%. (Kalpaklıo lu et al. 2004; Gülegen et al. 2005; Aykut et al. 2013b, 2013c; Zeytun et al.
2015, 2016). In adition, in our previous study (Zeytun et al. 2017), we reported that prevalence of D.
pteronyssinus and D. farinae in the homes of patients with allergic asthma was 84% and 16%,
respectively. In the present work, prevalence of D. pteronyssinus and D. farine in the homes of the
patients with AR was detected as 95.7% and 26.1%, respectively. All these studies show that D.
pteronyssinus is more prevalent than D. farine, and faunistic findings support that D. pteronyssinus
sensitivity in the SPT and serologic tests should be greater than D. farine sensitivity.
Unlike other studies, the present study compared SPT and serologic test results with mites in the
homes to detect D. pteronyssinus and D. farinae sensitivity of patients with AR. This is important
for a better understanding of the role HDMs play in allergic rhinitis aetiology. Dermatophagoides
pteronyssinus sensitivity of patients who had D. pteronyssinus in their homes were detected as 95.5%
according to SPT, and 27.3 according to IgE, and D. farinae sensitivity of patients with D. farinae
in their homes was detected as 83.3% according to SPT, and 50% according to IgE.
Dermatophagoides pteronyssinus sensitivity in the controls was detected as 12.5% according to SPT,
but D. farinae sensitivity was not detected, according to both SPT and mite-specific IgE results. Both
D. pteronyssinus and D. farinae sensitivity of patients who had presence of both mites in their homes
were detected as 80% according to SPT, and 40% according to IgE. But there were no controls who
had presence of both mite species in their homes and sensitivity to both mite species. But then there
were also controls who were not able to be detected sensitivity to these mites, despite there were D.
pteronyssinus or D. farinae in their homes. This situation may be due to cross-reactivity or false
negativity.
In our study, it was found that there was an increase in both specific IgE and total IgE levels of
patients based on the increase of mite density. This finding shows that there was a positive
correlation between between mite density in homes and serum IgE levels.
We should point out that a limited number of patients were included in the study due to the hight
cost of SPT and serological tests and this may have affected our results. In addition, cross-reactivity,
false negativity or positivity may have affected our findings.
In summary, the present study determined that patients with AR in Erzincan province were
sensitized to D. pteronyssinus and D. farinae, and that their homes contained both species of mites.
It may be helpful to consider these findings in clinical assessment of the patients with AR, and also
in treatment utilizing immunotherapy techniques.
Acknowledgement
We would like to thank the Erzincan University, Coordinator of Scientific Research Projects, which
suported this study (Project : FEN-A-300614-0107), Erzincan University Ethics Committee
(Decision : 2014-02/06), the all volunteers who participated to this study, and anonymous
reviewers. This study is a part of the first author’s PhD thesis, and the experimental preliminary
findings of this work were presented at 19
th
National Congress of Parasitology and Echinococcosis,
held from October 5 to 9, 2015 in Erzurum, Turkey.
214
SYSTEMATIC & APPLIED ACAROLOGY VOL. 23
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Submitted: 18 Sept. 2017; accepted by Norman Fashing: 27 Dec. 2017; published: 5 Feb. 2018