Allergy Asthma Immunol Res.  2019 Jan;11(1):116-128. 10.4168/aair.2019.11.1.116.

Mugwort Pollen-Related Food Allergy: Lipid Transfer Protein Sensitization and Correlation With the Severity of Allergic Reactions in a Chinese Population

Affiliations
  • 1Department of Allergy, Peking Union Medical College Hospital, Chinese Academy of Medical Sciences & Peking Union Medical College, Beijing, China. doctoryinjia@163.com
  • 2Beijing Key Laboratory of Precision Medicine for Diagnosis and Treatment on Allergic Diseases, Beijing, China.

Abstract

PURPOSE
Little is known about the importance of lipid transfer protein (LTP) sensitization in China. In this study, we investigated the relationship between LTP sensitization and the severity of clinical symptoms in a population of patients with mugwort pollen-related food allergy.
METHODS
Food-induced symptoms were evaluated in 148 patients with mugwort pollen allergy by a standardized questionnaire. Specific immunoglobulin E (IgE) to Art v 1, Art v 3, Pru p 3, Ara h 9 and Cor a 8 were quantified by ImmunoCAP. Immunoblotting of peach extracts were performed with sera from peach-allergic patients.
RESULTS
In total, 72% (107/148) of the study population experienced food allergy. Forty-eight percent (51/107) of patients with mugwort pollen-related food allergy experienced at least 1 episode of food-induced anaphylaxis. Food allergy correlated with IgE reactivity to Art v 3, but not to Art v 1. Sensitization to Pru p 3, Ara h 9 or Cor a 8 was prevalent (80%, 69 or 63%, respectively) among individuals with food allergy. Food allergic patients with systemic reactions (SR) had higher values for Pru p 3, Ara h 9 and Cor a 8 than patients with oral allergy syndrome (OAS). Furthermore, the strong IgE reactivity detected in immunoblots of peach extracts indicated that Pru p 3 was the major allergen and was more prevalent in patients with SR than in patients with OAS (100% vs. 55%).
CONCLUSIONS
LTPs are major food allergens for mugwort pollen-related food allergy in China, and may contribute to SR.

Keyword

Lipid transfer protein; mugwort pollen allergy; food allergy

MeSH Terms

Allergens
Anaphylaxis
Artemisia*
Asian Continental Ancestry Group*
China
Food Hypersensitivity*
Humans
Hypersensitivity*
Immunoblotting
Immunoglobulin E
Immunoglobulins
Prunus persica
Rhinitis, Allergic, Seasonal
Allergens
Immunoglobulin E
Immunoglobulins

Figure

  • Fig. 1 Food sensitization in 107 individuals with mugwort pollen-related food allergy.

  • Fig. 2 Levels of total IgE and specific IgE to mugwort pollen, Art v 1 and Art v 3 were compared in FA (filled triangles, n = 107) and NFA (open circles, n = 41) patients. IgE, immunoglobulin E; FA, food-allergic; NFA, non-food-allergic.

  • Fig. 3 Comparison of levels of total IgE and specific IgE to mugwort pollen, Art v 1 and Art v 3 in predicting mugwort pollen-related food allergy. Art v 3-specific IgE had the largest area under ROC curve (AUC, 0.757; 95% CI, 0.662–0.852; P < 0.001) with reference to total IgE (AUC, 0.479; 95% CI, 0.379–0.578; P = 0.689), specific IgE to mugwort pollen (AUC, 0.705; 95% CI, 0.620–0.789; P < 0.001) and Art v 1 (AUC, 0.495; 95% CI, 0.397–0.593; P = 0.925). IgE, immunoglobulin E; ROC, receiver operating characteristic; AUC, area under the curve; CI, confidence interval.

  • Fig. 4 IgE levels of LTP (Pru p 3, Ara h 9 and Cor a 8) were compared among food (peach, peanut and hazelnut, respectively)-allergic patients with systemic reactions and oral allergy syndrome. IgE, immunoglobulin E; LTP, lipid transfer protein.

  • Fig. 5 ROC curve analysis for specific IgE to mugwort pollen, Art v 3, peach and its allergenic components in predicting systemic reactions to peach. Pru p 3-specific IgE had the largest area under ROC curve (AUC, 0.77; 95% CI, 0.676–0.872; P < 0.001) with reference to specific IgE to mugwort pollen (AUC, 0.57; 95% CI, 0.448–0.693; P = 0.271), Art v 3 (AUC, 0.55; 95% CI, 0.420–0.670; P = 0.483), peach (AUC, 0.73; 95% CI, 0.627–0.837; P < 0.001), Pru p 1 (AUC, 0.48; 95% CI, 0.347–0.604; P = 0.701), and Pru p 4 (AUC, 0.58; 95% CI, 0.457–0.708; P = 0.199). ROC, receiver operating characteristic; IgE, immunoglobulin E; AUC, area under the curve; CI, confidence interval.

  • Fig. 6 Representative results of immunoblotting of peach extracts with sera from patients with mugwort pollen-related peach allergy. lane 1–6: serum from patients with systemic reactions to peach; lane 7–9: serum from patients with oral allergy syndrome; lane 10: serum from patients with mugwort pollinosis without food allergy.


Cited by  1 articles

Revised Pollen Calendar in Korea
Jung-Won Park
Allergy Asthma Immunol Res. 2020;12(2):171-172.    doi: 10.4168/aair.2020.12.2.171.


Reference

1. Ye S, Zhang J, Gu R. Investigation of aeroborne allergenic pollens in different regions of China. 1st edition. Beijing: Beijing Publishers;1991.
2. Popescu FD. Cross-reactivity between aeroallergens and food allergens. World J Methodol. 2015; 5:31–50.
Article
3. Webber CM, England RW. Oral allergy syndrome: a clinical, diagnostic, and therapeutic challenge. Ann Allergy Asthma Immunol. 2010; 104:101–108.
Article
4. Ballmer-Weber BK, Hoffmann A, Wüthrich B, Lüttkopf D, Pompei C, Wangorsch A, et al. Influence of food processing on the allergenicity of celery: DBPCFC with celery spice and cooked celery in patients with celery allergy. Allergy. 2002; 57:228–235.
Article
5. Figueroa J, Blanco C, Dumpiérrez AG, Almeida L, Ortega N, Castillo R, et al. Mustard allergy confirmed by double-blind placebo-controlled food challenges: clinical features and cross-reactivity with mugwort pollen and plant-derived foods. Allergy. 2005; 60:48–55.
Article
6. Pastorello EA, Pravettoni V, Farioli L, Rivolta F, Conti A, Ispano M, et al. Hypersensitivity to mugwort (Artemisia vulgaris) in patients with peach allergy is due to a common lipid transfer protein allergen and is often without clinical expression. J Allergy Clin Immunol. 2002; 110:310–317.
Article
7. Wen Z, Ye S. A report of 50 patients with artemisia pollenosis and plant food allergy. Zhonghua Yi Xue Za Zhi. 2002; 82:626–629.
8. Egger M, Mutschlechner S, Wopfner N, Gadermaier G, Briza P, Ferreira F. Pollen-food syndromes associated with weed pollinosis: an update from the molecular point of view. Allergy. 2006; 61:461–476.
Article
9. Ma S, Yin J, Jiang N. Component-resolved diagnosis of peach allergy and its relationship with prevalent allergenic pollens in China. J Allergy Clin Immunol. 2013; 132:764–767.
Article
10. Fernández-Rivas M, Bolhaar S, González-Mancebo E, Asero R, van Leeuwen A, Bohle B, et al. Apple allergy across Europe: how allergen sensitization profiles determine the clinical expression of allergies to plant foods. J Allergy Clin Immunol. 2006; 118:481–488.
Article
11. Sampson HA, Muñoz-Furlong A, Campbell RL, Adkinson NF Jr, Bock SA, Branum A, et al. Second symposium on the definition and management of anaphylaxis: summary report--second National Institute of Allergy and Infectious Disease/Food Allergy and Anaphylaxis Network symposium. Ann Emerg Med. 2006; 47:373–380.
Article
12. Bousquet J, Heinzerling L, Bachert C, Papadopoulos NG, Bousquet PJ, Burney PG, et al. Practical guide to skin prick tests in allergy to aeroallergens. Allergy. 2012; 67:18–24.
13. Pastorello EA, Farioli L, Pravettoni V, Ortolani C, Ispano M, Monza M, et al. The major allergen of peach (Prunus persica) is a lipid transfer protein. J Allergy Clin Immunol. 1999; 103:520–526.
Article
14. Flores E, Cervera L, Sanz ML, Diaz-Perales A, Fernández J. Plant food allergy in patients with pollinosis from the Mediterranean area. Int Arch Allergy Immunol. 2012; 159:346–354.
Article
15. Geroldinger-Simic M, Zelniker T, Aberer W, Ebner C, Egger C, Greiderer A, et al. Birch pollen-related food allergy: clinical aspects and the role of allergen-specific IgE and IgG4 antibodies. J Allergy Clin Immunol. 2011; 127:616–622.e1.
Article
16. Skypala IJ, Calderon MA, Leeds AR, Emery P, Till SJ, Durham SR. Development and validation of a structured questionnaire for the diagnosis of oral allergy syndrome in subjects with seasonal allergic rhinitis during the UK birch pollen season. Clin Exp Allergy. 2011; 41:1001–1011.
Article
17. Werfel T, Asero R, Ballmer-Weber BK, Beyer K, Enrique E, Knulst AC, et al. Position paper of the EAACI: food allergy due to immunological cross-reactions with common inhalant allergens. Allergy. 2015; 70:1079–1090.
Article
18. Gruber P, Gadermaier G, Bauer R, Weiss R, Wagner S, Leonard R, et al. Role of the polypeptide backbone and post-translational modifications in cross-reactivity of Art v 1, the major mugwort pollen allergen. Biol Chem. 2009; 390:445–451.
Article
19. Gao ZS, Yang ZW, Wu SD, Wang HY, Liu ML, Mao WL, et al. Peach allergy in China: a dominant role for mugwort pollen lipid transfer protein as a primary sensitizer. J Allergy Clin Immunol. 2013; 131:224–226.e1-3.
20. Lombardero M, García-Sellés FJ, Polo F, Jimeno L, Chamorro MJ, García-Casado G, et al. Prevalence of sensitization to Artemisia allergens Art v 1, Art v 3 and Art v 60 kDa. Cross-reactivity among Art v 3 and other relevant lipid-transfer protein allergens. Clin Exp Allergy. 2004; 34:1415–1421.
Article
21. García-Sellés FJ, Díaz-Perales A, Sánchez-Monge R, Alcántara M, Lombardero M, Barber D, et al. Patterns of reactivity to lipid transfer proteins of plant foods and Artemisia pollen: an in vivo study. Int Arch Allergy Immunol. 2002; 128:115–122.
22. Palacín A, Cumplido J, Figueroa J, Ahrazem O, Sánchez-Monge R, Carrillo T, et al. Cabbage lipid transfer protein Bra o 3 is a major allergen responsible for cross-reactivity between plant foods and pollens. J Allergy Clin Immunol. 2006; 117:1423–1429.
23. Mothes-Luksch N, Raith M, Stingl G, Focke-Tejkl M, Razzazi-Fazeli E, Zieglmayer R, et al. Pru p 3, a marker allergen for lipid transfer protein sensitization also in Central Europe. Allergy. 2017; 72:1415–1418.
Article
24. Scala E, Till SJ, Asero R, Abeni D, Guerra EC, Pirrotta L, et al. Lipid transfer protein sensitization: reactivity profiles and clinical risk assessment in an Italian cohort. Allergy. 2015; 70:933–943.
Article
25. Tolkki L, Alanko K, Petman L, Skydtsgaard MB, Milvang PG, Seppälä U, et al. Clinical characterization and IgE profiling of birch (Betula verrucosa)--allergic individuals suffering from allergic reactions to raw fruits and vegetables. J Allergy Clin Immunol Pract. 2013; 1:623–631.e1.
Article
26. Datema MR, Zuidmeer-Jongejan L, Asero R, Barreales L, Belohlavkova S, de Blay F, et al. Hazelnut allergy across Europe dissected molecularly: A EuroPrevall outpatient clinic survey. J Allergy Clin Immunol. 2015; 136:382–391.
27. Pascal M, Muñoz-Cano R, Reina Z, Palacín A, Vilella R, Picado C, et al. Lipid transfer protein syndrome: clinical pattern, cofactor effect and profile of molecular sensitization to plant-foods and pollens. Clin Exp Allergy. 2012; 42:1529–1539.
Article
28. Yin J, Yue FM, Wang LL, He HJ, Xu T, Zhang HY, et al. The clinical study of the relationship between allergic rhinitis and allergic asthma in the patients with autumnal pollinosis. Zhonghua Yi Xue Za Zhi. 2005; 85:1683–1687.
29. Yin J, Yue FM, Wang LL, He HJ, Xu T, Li H, et al. Natural course from rhinitis to asthma in the patients with autumnal pollinosis: a clinical study of 1096 patients. Zhonghua Yi Xue Za Zhi. 2006; 86:1628–1632.
30. Uasuf CG, Villalta D, Conte ME, Di Sano C, Barrale M, Cantisano V, et al. Different co-sensitizations could determine different risk assessment in peach allergy? Evaluation of an anaphylactic biomarker in Pru p 3 positive patients. Clin Mol Allergy. 2015; 13:30.
Article
31. Le TM, van Hoffen E, Lebens AF, Bruijnzeel-Koomen CA, Knulst AC. Anaphylactic versus mild reactions to hazelnut and apple in a birch-endemic area: different sensitization profiles? Int Arch Allergy Immunol. 2013; 160:56–62.
Article
32. Scheurer S, Lauer I, Foetisch K, San Miguel Moncin M, Retzek M, Hartz C, et al. Strong allergenicity of Pru av 3, the lipid transfer protein from cherry, is related to high stability against thermal processing and digestion. J Allergy Clin Immunol. 2004; 114:900–907.
Article
33. Offermann LR, Schlachter CR, Perdue ML, Majorek KA, He JZ, Booth WT, et al. Structural, functional, and immunological characterization of profilin panallergens Amb a 8, Art v 4, and Bet v 2. J Biol Chem. 2016; 291:15447–15459.
Article
34. Ganglberger E, Radauer C, Grimm R, Hoffmann-Sommergruber K, Breiteneder H, Scheiner O, et al. N-terminal sequences of high molecular weight allergens from celery tuber. Clin Exp Allergy. 2000; 30:566–570.
Article
Full Text Links
  • AAIR
Actions
Cited
CITED
export Copy
Close
Share
  • Twitter
  • Facebook
Similar articles
Copyright © 2024 by Korean Association of Medical Journal Editors. All rights reserved.     E-mail: koreamed@kamje.or.kr