(Trouessart) and D. Farinae Hughes (Acari: Pyroglyphidae) Sensitivity in Patients with Allergic Rhinitis: a Comparative Study

Systematic & Applied Acarology 23(2): 404–404 (2018) ISSN 1362-1971 (print); http://dx.doi.org/10.11158/saa.23.2.17 ISSN 2056-6069 (online)

Erratum Correction: Evaluation of Dermatophagoides pteronyssinus (Trouessart) and D. farinae Hughes (Acari: Pyroglyphidae) sensitivity in patients with allergic rhinitis: a comparative study

ERHAN ZEYTUN1*, SALİH DOĞAN1, EDHEM ÜNVER2 & FATİH ÖZÇİÇEK3 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: [email protected]

The authors are sorry that they made a mistake in spelling the family name of the first author on line 4 of page 206 in Zeytun et al. (2018): EYTUN should be ZEYTUN. This type error is evident in the paper itself because the running title in the footer of page 207 has the correct name: “ZEYTUN ET AL.: SENSITIVITY TO HDMS IN PATIENTS WITH ALLERGIC RHINITIS”.

Reference

Zeytun1, E., Doğan, S., Ünver, E. & Özçiçek, F. (2018) Evaluation of Dermatophagoides pteronyssinus (Trouessart) and D. farinae Hughes (Acari: Pyroglyphidae) sensitivity in patients with allergic rhinitis: a comparative study. Systematic & Applied Acarology, 23(2), 206–215. https://doi.org/10.11158/saa.23.2.2

Published: 22 Feb. 2018

1. Not “Eytun”

404 © Systematic & Applied Acarology Society Systematic & Applied Acarology 23(2): 206–215 (2018) ISSN 1362-1971 (print) http://doi.org/10.11158/saa.23.2.2 ISSN 2056-6069 (online)

Article

Evaluation of Dermatophagoides pteronyssinus (Trouessart) and D. farinae Hughes (Acari: Pyroglyphidae) sensitivity in patients with allergic rhinitis: a comparative study

ERHAN EYTUN1*, SALİH DOĞAN1, EDHEM ÜNVER2 & FATİH ÖZÇİÇEK3 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: [email protected]

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

206 © Systematic & Applied Acarology Society 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.

2018 ZEYTUN ET AL.: SENSITIVITY TO HDMS IN PATIENTS WITH ALLERGIC RHINITIS 207 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.

Patients Controls P value Age (Years) 32 (16–60) 25 (17–69) >0.05 a Median (min – max)] Sex <0.05 b Female 17 (73.9%) 10 (35.7%) Male 6 (26.1%) 18 (64.3%) 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.

Patients Controls P value SPT positivity D. pteronyssinus 21/23 (91.3%) 11/28 (39.3%) <0.001a D. farinae 10/23 (43.5%) 7/28 (25%) 0.164a Specific IgE positivity D. pteronyssinus 7/23 (30.4%) 0/28 (0%) 0.002a D. farinae 8/23 (34.8%) 0/28 (0%) 0.001a Total IgE level Normal (≤87 U/mL) 14/23 (60.9%) 25/28 (89.3%) 0.017a High (≥87 U/mL) 9/23 (39.1%) 3/28 (10.7%) Mean (min-max) 254.1 (1-1400) 51.4 (1.5-310) 0.048b

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)),

208 SYSTEMATIC & APPLIED ACAROLOGY VOL. 23 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

2018 ZEYTUN ET AL.: SENSITIVITY TO HDMS IN PATIENTS WITH ALLERGIC RHINITIS 209 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.

Homes of Patients Homes of Controls P value Total (specific-mite) Mite positive 23/23 (100%) 10/28 (35.7%) <0.001b a Mean mite (dust/g) 43.5 3.9 <0.001c a Total mite (dust/g) 1001 39 D. pteronyssinus Mite positive 22/23 (95.7%) 8/28 (28.6%) <0.001b a Mean mite (dust/g) 44.4 4.4 <0.001c a Total mite (dust/g) 977 35 D. farinae Mite positive 6/23 (26.1%) 2/28 (7.1%) 0.064b a Mean mite (dust/g) 4.0 2.0 0.068c a Total mite (dust/g) 24 4 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 Eskişehir (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

210 SYSTEMATIC & APPLIED ACAROLOGY VOL. 23 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.

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

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 Eskişehir 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-

2018 ZEYTUN ET AL.: SENSITIVITY TO HDMS IN PATIENTS WITH ALLERGIC RHINITIS 211 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.

P value a P value a Patients Controls (r) (r) Mite density (dust/g) 7 0 Median (min – max) (1–628) < 0.001 (0–8) 0.287 Specific IgE levels (kUA/L) 0.20 (0.751) 0.10 (-0.208) Median (min – max) (0.05–3.90) (0.05–0.030) Mite density (dust/g) 7 0 Median (min – max) (1–628) 0.010 (0–8) 0.338 Total IgE levels (U/mL) 58.2 (0.526) 19.7 (-0.188) Median (min – max) (7.1–1400) (1.5–310) 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

212 SYSTEMATIC & APPLIED ACAROLOGY VOL. 23 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%. (Kalpaklıoğlu 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 19th National Congress of Parasitology and Echinococcosis, held from October 5 to 9, 2015 in Erzurum, Turkey.

2018 ZEYTUN ET AL.: SENSITIVITY TO HDMS IN PATIENTS WITH ALLERGIC RHINITIS 213 References

Akdemir, C. & Yılmaz, S. (2009) Sensitization to house-dust mite and mite fauna in selected children's homes in Kutahya, Turkey. The Turkish Journal of Pediatrics, 51, 232–237. Akkaya, A., Ünlü, M. & Uygun, N. (1995) Evoluation of prick test positivity and total IgE levels in cases with allergic asthma and allergic rhinitis in Isparta district. Süleyman Demirel Üniversitesi Tıp Fakültesi Dergisi, 2, 29–32. (article in Turkish with an abstract in English) Al-Tamemi, S.H., Al-Shidhani, A.N., Al-Abri, R.K., Jothi, B., Al-Rawas, O.A. & Al-Riyami, B.M. (2008) The pattern of sensitisation to inhalant allergens in Omani patients with asthma, allergic rhinitis and rhinoconjunctivitis. Sultan Qaboos University Medical Journal, 8, 319–324. Atambay, M., Aycan, Ö.M., Yoloğlu, S., Karaman, U. & Daldal, N. (2006) The relationship between the skin allergy test and house dust mites. Turkish Journal of Parasitology, 30, 327–329. (article in Turkish with an abstract in English) Aykut, M., Erman, K. & Doğan, S. (2013a) Seasonal changes of house dust mite population in Bitlis and Muş provinces of Turkey. Turkish Journal of Parasitology, 37, 113–117. https://doi.org/10.5152/tpd.2013.26 Aykut, M., Erman, K., Doğan, S. & Ayyıldız, N. (2013b) House dust mites of Bitlis and Muş provinces. Turkish Bulletin of Entomology, 3, 169–177. (article in Turkish with an abstract in English) Aykut, M., Erman, K. & Doğan, S. (2013c) Prevalence of house dust mites in houses, hotels and student dormitories of Diyarbakır province. Dicle University Institute of Natural and Applied Science Journal, 2(1), 41–47. (article in Turkish with an abstract in English) Aykut, M., Erman, K. & Doğan, S. (2016) Variability in population density of house dust mites of Bitlis and Mus, Turkey. Journal of Medical Entemology, 53(3), 513–518. https://doi.org/10.1093/jme/tjw009 Boquete, M., Iraola, V., Fernandez-Caldas, E., Villaroel, L.A., Carballada, F.J., de la Cuesta, C.G., Lopez-Rico, M.R., Orjales, R.N., Parra, A., Soto-Mera, M.T., Varela, S. & Vidal, C. (2006) House dust mite species and allergen levels in Galicia, Spain: a cross-sectional, multicenter, comparative study. Journal of Investigational Allergology and Clinical Immunol- ogy, 16, 169–176. Bousquet, J., Khaltaev, N., Cruz A.A., Denburg, J., Fokkens, W., Togias, A., Zuberbier, T., Beana-Cagnani, C., Cononica, W.G., van Well, C., Agache, I., Ait-Khaled, N., Bachert, C., Blaiss, M., Bonini, S., Boulet, L.P., Bousquet, P.J., Camar- gos, P., Carlsen, K.H., Custovic, A., Chen, Y., Dahl, R., Demoly, P., Douagui, H., Durham, S., van Wijk, R.G., Kalayci, Ö., Kaliner, M., Kim, Y.Y., Kowalski, M.L., Kuna, P., Lemiere, C., Lan, L.T.T., Li, J., Lockey, R., Mavale, S., Meltzer, E.O., Mohammad, Y., Mullol, J., Naclerio, R., O’Hehir, R., Ohta, K., Ouedraogo, S., Palkonen, S., Papadopoulos, N., Passalacqua, G., Pawankar, R., Popov, T., Rabe, K., Rosado-Pinto, J., Scadding, G., Simons, F.E.R., Toskala, E., Valo- virta, E., van Cauwenberge, P., Wang, D.Y., Wickman, M., Yawn, B., Yorgancioglu, A., Yusuf, O. & Zar, H. (2008) ARIA (Allergic rhinitis and its impact on asthma) 2008 update (In collaboration with the World Health Organization, GA2LEN and AllerGen). Allergy, 86, 8–134. Calderon, M.A., Linneberg, A., Kleine-Tebbe, J., de Blay, F., de Rojas D.H.F., Virchow, J.C. & Demoly, P. (2015) Respiratory allergy caused by house dust mites: What do we really know? Journal of Allergy and Clinical Immunology, 136, 38–48. https://doi.org/10.1016/j.jaci.2014.10.012 Calvo, M., Fernandez-Caldas, E., Arellano, P., Marin, F., Carnes, J. & Hormaechea, A. (2005) Mite allergen exposure, sensitisation and clinical symptoms in Valdivia, Chile. Journal of Investigational Allergology and Clinical Immunology, 15, 189–196. Chew, G.L., Reardon, A.M., Correa, J.C., Young, M., Acosta, L., Mellins, R., Chew, F.T. & Perzanowski, M.S. (2009) Mite sensitization among Latina women in New York, where dust-mite allergen levels are typically low. Indoor Air, 19, 193– 197. https://doi.org/10.1111/j.1600-0668.2008.00578.x Çiftci, İ.H., Çetinkaya, Z., Aktepe, O.C., Kıyıldı, N., Aycan, O.M., Atambay, M. & Altındiş, M. (2004) The relation between house dust allergens and specific IgE. The Medical Journal of Kocatepe, 5, 29–32. (article in Turkish with an abstract in English) Colloff, M.-J. (2009) Dust mites. New Zealand and Australia, Csiro Publishing, 592 pp. Güleğen, E., Girişgin, O., Kütükoğlu, F., Girişgin, A.O. & Coşkun, S.Z. (2005) Mite species found in house dust in houses in Bursa. Turkish Journal of Parasitology, 29, 185–187. (article in Turkish with an abstract in English) Harmancı, E., Us, T., Özdemir, N., Akgün, Y., Aydınlı, A. & Mutlu, S. (2000) The relationship between skin prick tests and serum specific IgE which is determined by chemiluminescence method in the diagnosis of respiratory system allergies. The Turkish Respiratory Journal, 2, 31–35. (article in Turkish with an abstract in English) Ho, T.M., Murad, S., Kesavapillai, R. & Singaram, S.P. (1995) Prevalence of allergy to some inhalants among rhinitis patients in Malaysia. Asian Pacific Journal of Allergy and Immunology, 13, 11–16.

214 SYSTEMATIC & APPLIED ACAROLOGY VOL. 23 Kalpaklıoğlu, A.F., Emekci, M., Ferizli, A.G. & Mısırlıgil, Z. (2004). A survey of acarofauna in Turkey: comparison of seven different geographic regions. Allergy and Asthma Proceedings, 25, 185–190. Kim, H.S., Kang, S.H., Won, S., Lee, E.K., Chun, Y.H., Yoon, J.S., Kim, H.H. & Kim, J.T. (2015) Immunoglobulin E to allergen components of house dust mite in Korean children with allergic disease. Asia Pacific Allergy, 5, 156–162. https://doi.org/10.5415/apallergy.2015.5.3.156 Öztürk, O., Tokmak, A., Güçlü, E., Yıldızbaş, S. & Gültekin, E. (2005) Skin prick test results of patients with allergic rhinitis in Düzce. Düzce Medical Journal, 1, 11–14. (article in Turkish with an abstract in English) Pagan, J.A., Huertas, A.J., Iraola, V., Pinto, H., Martinez, R., Ramirez, M., Martos, M.D. & Carnes, J. (2012) Mite exposure in a Spanish Mediterranean region. Allergologia et Immunopathologia, 40, 92–99. https://doi.org/10.1016/j.aller.2011.02.008 Pumhirun, P., Towiwat, P. & Mahakit, P. (1997) Aeroallergen sensitivity of Thai patients with allergic rhinitis. Asian Pacific Journal of Allergy and Immunology, 15, 183–185. Sanchez-Borges, M., Fernandez-Caldas, E., Capriles-Hulett, A. & Caballero-Fonseca, F. (2014) Mite hypersensitivity in patients with rhinitis and rhinosinusitis living in a tropical environment. Allergologia et Immunopathologia, 42, 120– 126. https://doi.org/10.1016/j.aller.2012.07.011 Seedat, R.Y., Claassen, J., Claassen, A.J. & Joubert, G. (2010) Mite and cockroach sensitisation in patients with allergic rhinitis in the Free State. South African Medical Journal, 100, 160–163. https://doi.org/10.7196/SAMJ.3669 Somorin, A.O., Hunponu-Wusu, O.O., Mumcuoğlu, K.Y. & Heiner, D.C. (1978) Mite allergy in Nigerians: studies on house dust mites in houses of allergic patients in Lagos. Irish Journal of Medical Science, 147, 26–30. https://doi.org/10.1007/BF02939363 Spieksma, F.T. (1997) Domestic mites from an acarologic perspective. Allergy, 52, 360–368. https://doi.org/10.1111/j.1398-9995.1997.tb01012.x Valmonte, G.R., Cauyan, G.A. & Ramos, J.D.A. (2012) IgE cross-reactivity between house dust mite allergens and Ascaris lumbricoides antigens. Asia Pacific Allergy, 2, 35–44. https://doi.org/10.5415/apallergy.2012.2.1.35 Vartiainen, E., Petays, T., Haahtela, T., Jousilahti, P. & Pekkanen, J. (2002) Allergic diseases, skin prick test responses, and IgE levels in North Karelia, Finland, and the Republic of Karelia, Russia. Journal of Allergy and Clinical Immunology, 109, 643–648. https://doi.org/10.1067/mai.2002.123307 Vidal-Quist J.C., Ortego, F., Lombardero, M., Castanera, P. & HernandezVCrespo, P. (2015) Allergen expression in the Euro- pean house dust mite Dermatophagoides pteronyssinus throughout development and response to environmental condi- tions. Medical and Veterinary Entomology, 29, 137–146. https://doi.org/10.1111/mve.12102 Yasan, H., Aynalı, G., Akkuş, O., Doğru, H., Özkan, M. & Sahin, M. (2006) Variaton and symptomatic correlation of allergen profile responsible for allergic rhinitis. KBB Forum, 5, 158–160. (article in Turkish with an abstract in English) Yılmaz, N., Can, D., Asilsoy, S. & Gülle, S. (2009) The diagnostic value of specific IgE in allergic diseases. Asthma Allergy Immunology, 7, 111–117. (article in Turkish with an abstract in English) Zeytun, E., Doğan, S., Aykut, M., Özçiçek, F., Ünver, E. & Özçiçek, A. (2015) House dust mites in Erzincan province. Turkish Journal of Parasitology, 39, 124–130. https://doi.org/10.5152/tpd.2015.3759 Zeytun, E., Doğan, S., Özçiçek, F., Ünver, E. & Dilkaraoğlu, S. (2016) Comparison of living and bedrooms in terms of house dust mites in the province of Erzincan, Turkey. Journal of Medical Entemology, 53(1), 26–30. https://doi.org/10.1093/jme/tjv186 Zeytun, E., Doğan, S., Özçiçek, F. & Ünver, E. (2017) Sensitivity to house dust mites allergens in patients with allergic asthma in Erzincan province, Turkey. Turkish Journal of Parasitology, 41, 34–41. https://doi.org/10.5152/tpd.2017.5059 Zhang, Z.-Q., Fan, Q.-H., Pesic, V., Smit, H., Bochkov, A.V., Khaustov, A.A., Baker, A., Wohltmann, A., Wen, T., Amrine, J.W., Beron, P., Lin, J., Gabrys, G. & Husband, R. (2011) Order Trombidiformes Reuter, 1909. In: Zhang, Z.-Q. (Ed.) Animal biodiversity: An outline of higher-level classification and survey of taxonomic richness. Zootaxa, 3148, 129– 138. Zhang, C., Li, J., Lai, X., Zheng, Y., Gjesing, B., Spangford, M.D. & Zhong, N. (2012) House dust mite and storage mite IgE reactivity in allergic patients from Guangzhou, China. Asian Pacific Journal of Allergy and Immunology, 30, 294–300.

Submitted: 18 Sept. 2017; accepted by Norman Fashing: 27 Dec. 2017; published: 5 Feb. 2018

2018 ZEYTUN ET AL.: SENSITIVITY TO HDMS IN PATIENTS WITH ALLERGIC RHINITIS 215