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Original paper

The importance of specific IgE antibodies in the epidemiology of allergic rhinitis and asthma (ECAP survey): part five. The relationship between the concentration of specific IgE antibodies in serum and types of rhinitis

Andrzej Namysłowski
1
,
Agnieszka Lipiec
1
,
Wojciech Zieliński
1, 2
,
Filip Raciborski
1
,
Edyta Krzych-Fałta
1
,
Krzysztof Samoliński
3
,
Anna Szylling
4
,
Bolesław Samoliński
1

  1. Department of the Prevention of Environmental Hazards, Allergology and Immunology, Medical University of Warsaw, Warsaw, Poland
  2. Department of Econometrics and Statistics, Warsaw University of Life Sciences, Warsaw, Poland
  3. Department of Emergency Medical Services, Medical University of Warsaw, Warsaw, Poland
  4. Department of Allergology and Clinical Immunology of the Central Clinical Hospital, Warsaw, Poland
Adv Dermatol Allergol 2023; XL (5): 617-624
Online publish date: 2023/08/04
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Introduction

Epidemiological observations from the last decades demonstrate a rise in the incidence of allergic rhinitis and asthma in developed countries [1]. They are currently diseases with major prevalence and morbidity rates for people under 30 years old suffering from non-infectious chronic diseases [25]. Numerous studies were performed as part of the Epidemiology of Allergic Diseases in Poland (ECAP) survey, proving the epidemiological significance of these diseases and great diversity of allergy risk factors [69]. Determination of specific IgE in respondents’ serum, a reliable method to evaluate allergic hypersensitivity [10, 11], supplements the results of this survey [12].

Aim

The aim of the study was to determine the relationship between the concentration of specific IgE antibodies in serum and types of rhinitis.

Material and methods

The quantitative data presented in the article were collected as part of the Epidemiology of Allergic Diseases in Poland (ECAP) project and its continuation. The ECAP comprised 2 main phases: (i) a questionnaire-based study (computer-assisted personal interview – CAPI); and (ii) a complementary clinical assessment (spirometry with bronchodilator challenge, skin-prick tests, peak nasal inspiratory flow, and blood sampling for genetic and immune tests). A total of 18,617 individuals from 8 cities (each with a population in excess of 150,000) and one rural region took part in the study (phase one). The sample was drawn (by stratified cluster sampling method) from a personal identity number (PESEL) database (maintained by the Minister of the Interior and Administration). 4783 respondents were randomly selected and examined by allergists (phase 2 of the study). Blood from 4077 respondents was collected, and the concentration of sIgE antibodies against allergens d1 (Dermatophagoides pteronyssinus), e1 (cat dander), g6 (timothy grass), and m6 (Alternaria alternata) was determined in serum, using the reference method CAP (Phadia reagents, UniCAP 100 laboratory system). A concentration of sIgE antibodies of at least 0.35 IU/ml (classes 1–6) or 0.7 IU/ml (classes 2–6) was considered positive. The sIgE-determined respondents included 2223 females and 1854 males. 1026 respondents were aged 6–7 years, 1153 respondents were aged 13–14 years, and 1898 respondents were adults. An exact methodology of the ECAP survey is described at www.ecap.pl [12] and in the "Polish Journal of Allergology" [13].

The results of determination of sIgE antibodies were correlated as follows:

  • to the following clinical diagnoses: healthy , intermittent allergic rhinitis, persistent allergic rhinitis, nonallergic rhinitis, seasonal allergic rhinitis, perennial allergic rhinitis, nasal polyps;

  • to results of skin-prick tests: negative (0–2 mm), + (3–5 mm), ++ (6–8 mm), +++ (at least 9 mm).

Statistical analysis

The aim of the statistical analysis was to compare proportions of people with a high level of immunoglobulin in 2 groups. The classical approximate test for comparison of 2 proportions was applied [14]. If the calculated p-value was less than 0.05, a statistically significant difference between the investigated proportions was recognised. Otherwise, the fractions of people with a high level of immunoglobulin in the investigated groups was treated as similar. Calculations were performed using the statistical package Statistica (Statistica, Tulsa, Oklahoma, US).

Results

In respondents with allergic rhinitis, sIgE antibodies against D. pteronyssinus and timothy grass were the most frequently detected (“D. pteronyssinus” vs. “cat dander”, classes 1–6 p < 0.001, classes 2–6 p < 0.001; “timothy grass” vs. “cat dander”, classes 1–6 p < 0.001, classes 2–6 p < 0.001). In the same group, sIgE antibodies against A. alternata were the least frequently detected (“A. alternata” vs. “cat dander”, classes 1–6 p < 0.001, classes 2–6 p < 0.005) (Table 1).

Table 1

Number (percentage) of respondents with sIgE concentration ≥ 0.35 IU/ml (classes 1–6) or ≥ 0.7 IU/ml (classes 2–6) – respondents with allergic rhinitis

ClassesRespondents’ sIgE against, n (%)
D. pteronyssinus (d1)Cat dander (e1)Timothy grass (g6)A. alternata (m6)N (100%)
1–6390 (34.6)176 (15.6)394 (35.0)106 (9.4)1127
2–6329 (29.2)127 (11.3)327 (29.0)88 (7.8)1127

sIgE antibodies against any allergen were detected in 60.1% (classes 1–6)/53.3% (classes 2–6) of respondents with allergic rhinitis, but also in 9.9% (classes 1–6)/7.6% (classes 2–6) of healthy respondents.

sIgE antibodies against D. pteronyssinus were more frequently detected in respondents with persistent allergic rhinitis than in respondents with intermittent allergic rhinitis (classes 1–6 p < 0.001, classes 2–6 p < 0.001), relating to sIgE antibodies against cat dander, this disparity is lower (classes 1–6 p < 0.1, classes 2–6 p < 0.1), relating to sIgE antibodies against A. alternata, no statistically significant differences were identified. sIgE antibodies against timothy grass were more frequently detected in respondents with intermittent allergic rhinitis than in respondents with persistent allergic rhinitis (classes 1–6 p < 0.05, classes 2–6 p < 0.05) (Table 2).

Table 2

Number (percentage) of respondents with sIgE concentration ≥ 0.35 IU/ml (classes 1–6) or ≥ 0.7 IU/ml (classes 2–6) – respondents with intermittent, persistent, seasonal, or perennial allergic rhinitis

ClassesRespondents’ sIgE against, n (%)
D. pteronyssinus (d1)Cat dander (e1)Timothy grass (g6)A. alternata (m6)N (100%)
Intermittent allergic rhinitis:
 1–6110 (20.6)72 (13.5)206 (38.6)46 (8.6)534
 2–697 (18.2)51 (9.6)168 (31.5)36 (6.7)534
Persistent allergic rhinitis:
 1–6280 (47.2)104 (17.5)188 (31.7)60 (10.1)593
 2–6232 (39.1)76 (12.8)159 (26.8)52 (8.8)593
Seasonal allergic rhinitis:
 1–683 (24.2)67 (19.5)172 (50.2)34 (9.9)343
 2–668 (19.8)48 (14.0)150 (43.7)26 (7.6)343
Perennial allergic rhinitis:
 1–6159 (54.3)54 (18.4)70 (23.9)22 (7.5)293
 2–6133 (45.4)39 (13.3)55 (18.8)17 (5.8)293

sIgE antibodies against D. pteronyssinus were more frequently detected in respondents with perennial allergic rhinitis than in respondents with seasonal allergic rhinitis (classes 1–6 p < 0.001, classes 2–6 p < 0.001). sIgE antibodies against timothy grass were more frequently detected in respondents with seasonal allergic rhinitis than in respondents with perennial allergic rhinitis (classes 1–6 p < 0.001, classes 2–6 p < 0.001). Relating to allergens of cat dander and A. alternata, no statistically significant differences were identified (Table 2).

Relating to an allergen of timothy grass, sIgE antibodies were more frequently detected in respondents with intermittent allergic rhinitis than in healthy respondents, regardless of skin-prick test (negative, ++, +++ p < 0.005 to p < 0.001). Relating to allergens of D. pteronyssinus, cat dander, and A. alternata, sIgE antibodies were more frequently detected in respondents with intermittent allergic rhinitis and a negative skin-prick test as compared to healthy respondents with a negative skin-prick test (classes 1–6, D. pteronyssinus p < 0.005; classes 2–6 p < 0.005 to p < 0.001) (Table 3, Figure 1).

Table 3

Number (percentage) of respondents with sIgE concentration ≥ 0.35 IU/ml (classes 1–6) or ≥ 0.7 IU/ml (classes 2–6) – healthy respondents and respondents with intermittent or persistent allergic rhinitis

ClassesRespondents’ sIgE against, n (%)
D. pteronyssinus (d1)Cat dander (e1)Timothy grass (g6)A. alternata (m6)N (100%) – d1, e1, g6, m6
Healthy, skin-prick test negative:
 1–628 (1.7)14 (0.8)23 (1.4)4 (0.2)1683, 1797, 1710, 1817
 2–612 (0.7)3 (0.2)15 (0.9)1 (0.1)
Intermittent allergic rhinitis, skin-prick test negative:
 1–615 (4.3)6 (1.6)10 (4.3)3 (0.7)349, 376, 234, 433
 2–610 (2.9)5 (1.3)7 (3.0)3 (0.7)
Healthy, skin-prick test +:
 1–626 (20.3)128
 2–619 (14.8)
Intermittent allergic rhinitis, skin-prick test +:
 1–640 (30.5)131
 2–625 (19.1)
Healthy, skin-prick test ++:
 1–611 (45.8)24
 2–611 (45.8)
Intermittent allergic rhinitis, skin-prick test ++:
 1–692 (87.6)105
 2–675 (71.4)
Healthy, skin-prick test +++:
 1–611 (78.6)14
 2–610 (71.4)
Intermittent allergic rhinitis, skin-prick test +++:
 1–664 (100.0)64
 2–661 (95.3)
Healthy, skin-prick test negative:
 1–628 (1.7)14 (0.8)4 (0.2)1683, 1797, 1817
 2–612 (0.7)3 (0.2)1 (0.1)
Persistent allergic rhinitis, skin-prick test negative:
 1–618 (9.1)12 (3.0)6 (1.2)198, 400, 486
 2–610 (5.1)10 (2.5)4 (0.8)
Healthy, skin-prick test +:
 1–640 (28.0)14 (20.3)26 (20.3)143, 69, 128
 2–627 (18.9)10 (14.5)19 (14.8)
Persistent allergic rhinitis, skin-prick test +:
 1–6101 (46.1)51 (37.0)41 (34.2)219, 138, 120
 2–674 (33.8)31 (22.5)27 (22.5)
Healthy, skin-prick test ++:
 1–611 (45.8)24
 2–611 (45.8)
Persistent allergic rhinitis, skin-prick test ++:
 1–674 (80.6)92
 2–661 (66.3)
Healthy, skin-prick test +++:
 1–611 (78.6)14
 2–610 (71.4)
Persistent allergic rhinitis, skin-prick test +++:
 1–676 (96.2)79
 2–674 (93.7)
Figure 1

Percentage of respondents with sIgE concentration ≥ 0.35 IU/ml (classes 1–6) or ≥ 0.7 IU/ml (classes 2–6) – healthy respondents and respondents with intermittent or seasonal allergic rhinitis

/f/fulltexts/PDIA/51199/PDIA-40-51199-g001_min.jpg

Relating to allergens of D. pteronyssinus, cat dander, and A. alternata, sIgE antibodies were more frequently detected in respondents with persistent allergic rhinitis and a negative skin-prick test as compared to healthy respondents with a negative skin-prick test. Numerous statistically significant differences were identified (p < 0.005 to p < 0.001). Relating to allergens of D. pteronyssinus and cat dander, sIgE antibodies were more frequently detected in respondents with persistent allergic rhinitis and a weakly positive skin-prick test as compared to healthy respondents with a weakly positive skin-prick test. Numerous statistically significant differences were identified (p < 0.05 to p < 0.001). Relating to an allergen of timothy grass, sIgE antibodies were more frequently detected in respondents with persistent allergic rhinitis and a positive skin-prick test as compared to healthy respondents with a positive skin-prick test. Numerous statistically significant differences were identified (p < 0.05 to p < 0.001) (Table 3, Figure 2).

Figure 2

Percentage of respondents with sIgE concentration ≥ 0.35 IU/ml (classes 1–6) or ≥ 0.7 IU/ml (classes 2–6) – healthy respondents and respondents with persistent or perennial allergic rhinitis

/f/fulltexts/PDIA/51199/PDIA-40-51199-g002_min.jpg

Relating to an allergen of timothy grass, sIgE antibodies were more frequently detected in respondents with seasonal allergic rhinitis than in healthy respondents, regardless of skin-prick test result (negative, ++, +++ p < 0.05 to p < 0.001). Relating to allergens of D. pteronyssinus, cat dander, and A. alternata, sIgE antibodies were more frequently detected in respondents with seasonal allergic rhinitis and a negative skin-prick test as compared to healthy respondents with a negative skin-prick test result. Numerous statistically significant differences were identified (p < 0.05 to p < 0.005). Relating to an allergen of cat dander, sIgE antibodies were more frequently detected in respondents with seasonal allergic rhinitis and a weakly positive skin-prick test as compared to healthy respondents with a weakly positive skin-prick test (classes 1–6 p < 0.005, classes 2–6 p < 0.05) (Table 4, Figure 1). Relating to allergens of D. pteronyssinus and cat dander, sIgE antibodies were more frequently detected in respondents with perennial allergic rhinitis and a negative skin-prick test as compared to healthy respondents with a negative skin-prick test (p < 0.001) and in respondents with perennial allergic rhinitis and a weakly positive skin-prick test as compared to healthy respondents with a weakly positive skin-prick test (p < 0.05). Relating to an allergen of timothy grass, sIgE antibodies were more frequently detected in respondents with perennial allergic rhinitis and a medium or strongly positive skin-prick test as compared to healthy respondents with a medium or strongly positive skin-prick test result. Numerous statistically significant differences were identified (p < 0.05 to p < 0.005) (Table 4, Figure 2).

Table 4

Number (percentage) of respondents with sIgE concentration ≥ 0.35 IU/ml (classes 1–6) or ≥ 0.7 IU/ml (classes 2–6) – healthy respondents and respondents with seasonal or perennial allergic rhinitis

ClassesRespondents’ sIgE against, n (%)
D. pteronyssinus (d1)Cat dander (e1)Timothy grass (g6)A. alternata (m6)N (100%) – d1, e1, g6, m6
Healthy, skin-prick test negative:
 1–615 (1.4)10 (0.9)14 (1.3)2 (0.2)1109, 1162, 1120, 1186
 2–67 (0.6)4 (0.3)7 (0.6)1 (0.1)
Seasonal allergic rhinitis, skin-prick test negative:
 1–68 (4.1)6 (2.7)4 (3.8)3 (1.2)195, 220, 106, 261
 2–63 (1.5)5 (2.3)4 (3.8)2 (0.8)
Healthy, skin-prick test +:
 1–610 (16.7)20 (24.4)60, 82
 2–65 (8.3)14 (17.1)
Seasonal allergic rhinitis, skin-prick test +:
 1–629 (39.2)25 (32.9)74, 76
 2–616 (21.6)17 (22.4)
Healthy, skin-prick test ++:
 1–68 (38.1)21
 2–67 (33.3)
Seasonal allergic rhinitis, skin-prick test ++:
 1–664 (81.0)79
 2–652 (65.8)
Healthy, skin-prick test +++:
 1–69 (75.0)12
 2–68 (66.7)
Seasonal allergic rhinitis, skin-prick test +++:
 1–679 (96.3)82
 2–677 (93.9)
Healthy, skin-prick test negative:
 1–615 (1.4)10 (0.9)1109, 1162,
 2–67 (0.6)4 (0.3)
Perennial allergic rhinitis, skin-prick test negative
 1–615 (16.1)9 (4.4)93, 203
 2–611 (11.8)6 (3.0)
Healthy, skin-prick test +:
 1–625 (29.4)10 (16.7)85 , 60
 2–617 (20.0)5 (8.3)
Perennial allergic rhinitis, skin-prick test +:
 1–646 (46.5)29 (35.8)99, 81
 2–634 (34.3)18 (22.2)
Healthy, skin-prick test ++:
 1–68 (38.1)21
 2–67 (33.3)
Perennial allergic rhinitis, skin-prick test ++:
 1–636 (76.6)47
 2–629 (61.7)
Healthy, skin-prick test +++:
 1–69 (75.0)12
 2–68 (66.7)
Perennial allergic rhinitis, skin-prick test +++:
 1–634 (94.4)36
 2–633 (91.7)

Discussion

Numerous studies were performed as part of the ECAP survey, proving the epidemiological significance of these diseases and great diversity of allergy risk factors. Determination of specific IgE in serum of the respondents, the most reliable method to evaluate allergic hypersensitivity, has been the continuation of ECAP.

sIgE antibodies against D. pteronyssinus were more frequently detected in respondents with persistent allergic rhinitis than in respondents with intermittent allergic rhinitis. Relating to IgE antibodies against cat dander, this disparity is lower. Relating to sIgE antibodies against A. alternata, no statistically significant differences were identified. sIgE antibodies against timothy grass were more frequently detected in respondents with intermittent allergic rhinitis than in respondents with persistent allergic rhinitis. In a study by Corsico et al., specific IgE levels to house-dust mite were significantly higher in patients with persistent allergic rhinitis than in patients with intermittent allergic rhinitis [15]. On the other hand, in a study by Bauchau et al., subjects with persistent allergic rhinitis were more often sensitized to grass pollen, but less often to house dust mites, than subjects with intermittent allergic rhinitis [16]. Furthermore, in a study by Bousquet et al., most patients with intermittent allergic rhinitis had a pollen sensitivity, but 5% had a single house dust mite sensitization, and over 50% of patients with persistent allergic rhinitis were sensitized to pollens or house dust mites [17]. sIgE antibodies against D. pteronyssinus were more frequently detected in respondents with perennial allergic rhinitis than in respondents with seasonal allergic rhinitis. sIgE antibodies against timothy grass were more frequently detected in respondents with seasonal allergic rhinitis than in respondents with perennial allergic rhinitis. Relating to allergens of cat dander and A. alternata, no statistically significant differences were identified. In a study by Stoltz et al., sensitization to seasonal compared with perennial allergens was more closely associated with rhinitis risk [18]. In a study by Rolinck-Werninghaus et al., baseline specific IgE, but not total IgE, was associated with symptom severity during the pollen season in children with seasonal allergic rhinitis [19]. In a study by Hatzler et al., testing IgE sensitization at a preclinical stage facilitated prediction of seasonal allergic rhinitis [20]. On the other hand, in a study by Nickelsen et al., there was a lack of correlation between titres of serum or nasal secretory grass-specific IgE and symptoms in untreated patients with seasonal allergic rhinitis [21]. In the study reported in this article, sensitization to D. pteronyssinus increased the probability of persistent/perennial allergic rhinitis, and sensitization to timothy grass increased the probability of intermittent/seasonal allergic rhinitis. The lack of correlation between sensitization to cat dander and persistent/perennial allergic rhinitis presumably resulted from a seasonally variable indoor concentration of animal hair. Allergens of A. alternata are present indoors all year long, but their concentration fluctuates in particular months, which probably causes the lack of correlation between sensitization to A. alternata and persistent/perennial allergic rhinitis or intermittent/seasonal allergic rhinitis.

When sIgE antibodies against timothy grass were detected, the occurrence of intermittent/seasonal allergic rhinitis is much more probable. Relating to respondents with a negative skin-prick test with allergens of D. pteronyssinus, cat dander, or A. alternata, when sIgE antibodies against the same allergen were detected, the occurrence of intermittent/seasonal allergic rhinitis is much more probable. Therefore, it is worth determining specific IgE antibodies in patients with symptoms of intermittent or seasonal allergic rhinitis and negative skin-prick tests. The results of this determination enhance the likelihood of an accurate diagnosis.

Relating to respondents with a negative or weakly positive skin-prick test with allergens of D. pteronyssinus or cat dander, when sIgE antibodies against the same allergen were detected, occurrence of persistent/perennial allergic rhinitis was much more probable. Relating to respondents with a medium or strongly positive skin-prick test with an allergen of timothy grass, when sIgE antibodies against the same allergen were detected, occurrence of persistent/perennial allergic rhinitis was much more probable. Thus, it is worth determining specific IgE antibodies in patients with symptoms of persistent or perennial allergic rhinitis and a negative or weakly positive skin-prick test with allergens of D. pteronyssinus or cat dander. The results of this determination enhance the likelihood of an accurate diagnosis, as previously.

Conclusions

sIgE antibodies against any allergen are detected in 60.1% (classes 1–6)/53.3% (classes 2–6) of respondents with allergic rhinitis, but also in 9.9% (classes 1–6)/7.6% (classes 2–6) of healthy respondents. Relating to respondents with a negative skin-prick test, when sIgE antibodies against the same allergen are detected, occurrence of intermittent/seasonal allergic rhinitis is much more probable. Relating to respondents with a negative or weakly positive skin-prick test with allergens of D. pteronyssinus or cat dander, when sIgE antibodies against the same allergen are detected, occurrence of persistent/perennial allergic rhinitis is much more probable.

Acknowledgments

The study was approved by the institutional Bioethics Committee.

The study was performed as part of a research grant from the National Science Centre (Poland), 2011/01/B/NZ7/05289.

Conflict of interest

The authors declare no conflict of interest.

References

1 

Asher MI, Montefort S, Björkstén B, et al. Worldwide time trends in the prevalence of symptoms of asthma, allergic rhinoconjunctivitis, and eczema in childhood: ISAAC Phases One and Three repeat multicountry cross-sectional surveys. Lancet 2006; 368: 733-43.

2 

World Allergy Organization (WAO) White Book on Allergy. Pawankar R, Canonica GW, Holgate ST, Lockey RD (eds.). WAO, Milwaukee, Wisconsin 2011.

3 

Matricardi PM. The allergy epidemic. In: Global Atlas of Allergy. Akdis CA, Agache I (eds.). EEACI, Zurich, Switzerland 2014; 112-4.

4 

Bousquet J, Schünemann HJ, Samolinski B, et al. Allergic rhinitis and its impact on asthma (ARIA): achievements in 10 years and future needs. J Allergy Clin Immunol 2012; 130: 1049-62.

5 

Van Cauwenberge P, Watelet JB, Van Zele T, et al. Spreading excellence in allergy and asthma: the Gallen Project. Allergy 2005; 60: 858-64.

6 

Samoliński B, Sybilski A, Raciborski F, et al. Występowanie astmy oskrzelowej u dzieci, młodzieży i młodych dorosłych w Polsce w świetle badania ECAP. Alerg Astma Immun 2009; 14: 27-34.

7 

Samoliński B, Sybilski AJ, Raciborski F, et al. Prevalence of rhinitis in polish population according to the ECAP (Epidemiology of Allergic Disorders in Poland) study. Otolaryngol Pol 2009; 63: 324-30.

8 

Stankiewicz-Choroszucha B, Wawrzyniak Z, Lipiec A, et al. Consequences of smoke inhalation in the “Epidemiology of Allergic Diseases in Poland” project (ECAP). Ann Agric Environ Med 2011; 18: 420-8.

9 

Sybilski AJ, Raciborski F, Lipiec A, et al. Atopic dermatitis is a serious health problem in Poland. Epidemiology studies based on the ECAP study. Adv Dermatol Allergol 2015; 32: 1-10.

10 

Eriksson NE. Allergy screening with Phadiatop and CAP Phadiatop in combination with a questionnaire in adults with asthma and rhinitis. Allergy 1990; 45: 285-92.

11 

Brożek JL, Bousquet J, Agache I, et al. Allergic Rhinitis and its Impact on Asthma (ARIA) guidelines – 2016 revision. J Allergy Clin Immunol 2017; 140: 950-8.

12 

Epidemiologia chorób alergicznych w Polsce (ECAP). Available at: www.ecap.pl (Access 28.07.2021).

13 

Samoliński B, Raciborski F, Lipiec A, et al. Epidemiologia chorób alergicznych w Polsce (ECAP). Pol J Allergol 2014; 1: 10-18.

14 

Zieliński W. Wybrane testy statystyczne. Fundacja Rozwój SGGW. Warsaw, Poland 1999.

15 

Corsico AG, De Amici M, Ronzoni V, et al. Allergen-specific immunoglobulin E and allergic rhinitis severity. Allergy Rhinol 2017; 8: e1-e4.

16 

Bauchau V, Durham SR. Epidemiological characterization of the intermittent and persistent types of allergic rhinitis. Allergy 2005; 60: 350-3.

17 

Bousquet J, Annesi-Maesanow I, Caratz F, et al. Characteristics of intermittent and persistent allergic rhinitis: DREAMS study group. Clin Exp Allergy 2005; 35: 728-32.

18 

Stoltz DJ, Jackson DJ, Evans MD, et al. Specific patterns of allergic sensitization in early childhood and asthma & rhinitis risk. Clin Exp Allergy 2013; 43: 233-41.

19 

Rolinck-Werninghaus C, Keil T, Kopp M, et al. Specific IgE serum concentration is associated with symptom severity in children with seasonal allergic rhinitis. Allergy 2008; 63: 1339-44.

20 

Hatzler L, Panetta V, Lau S, et al. Molecular spreading and predictive value of preclinical IgE response to Phleum pratense in children with hay fever. J Allergy Clin Immunol 2012; 130: 894-901.

21 

Nickelsen JA, Georgitis JW, Reisman RE. Lack of correlation between titers of serum allergen-specific IgE and symptoms in untreated patients with seasonal allergic rhinitis. J Allergy Clin Immunol 1986; 77: 43-8.

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