Profile of cross-reactivity to common pollen allergens in Northwest China based on component resolved diagnosis | Scientific Reports

Scientific Reports volume 14, Article number: 24446 (2024) Cite this article

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The prevalence of allergic diseases such as Allergic Rhinitis and Asthma is steadily increasing globally, with pollen allergy being one of the most significant sensitizing factors. However, the cross-reactivity of different pollen allergies remains unclear, posing challenges in the diagnosis and treatment of individuals with multiple sensitivities. In this study, the Component Resolved Diagnosis technique was performed to simultaneously measure the specific IgE concentrations of 52 patients against Art v and its components (Art v 1), Phl p and its components (Phl p 1, Phl p 4, Phl p 5, Phl p 6, Phl p 7, Phl p 12), Bet v and its components (Bet v 1, Bet v 2), Amb a and its component (Amb a 1), and Amb p. Additionally, sIgE inhibition tests were conducted by Art v, Phl p, and Bet v extracts. Among Art v-positive patients, 64.6% showed positivity for Art v 1. In Phl p-positive patients, Phl p 12 had the highest positivity rate (75.0%). Among Bet v-positive patients, 75.6% exhibited positivity for Bet v 2, whereas for Amb a and Amb p-positive patients, 23.7% and 29.0% respectively showed positivity for Amb a 1. The sIgE inhibition assays results revealed that Art v extract had inhibition rates greater than 73.2% against Phl p and its component Phl p 12, as well as Bet v and its component Bet v 2. Simultaneously, Phl p extract showed inhibition rates of 80.70–89.87% against Phl p 12, Bet v and Bet v 2. Bet v extract showed inhibition rates ranging from 21.9 to 59.8% against Phl p and Bet v 2, with a better inhibition rate (76.80%) against Phl p 12. In conclusion, Art v 1 is identified as the principal component of Art v. The profilin proteins of Phl p and Bet v (Phl p 12 and Bet v 2), are implicated as potential cross-reactive elements contributing to polysensitization in patients with respiratory allergies in the Northwest region of China. This cross-reactivity leads to a shared sensitization mechanism among pollen allergens such as Art v, Phl p, and Bet v.

In recent years, the prevalence of allergic diseases such as allergic rhinitis (AR) and allergic asthma (AA) has been steadily increasing worldwide, affecting 10–40% of the global population. Allergic diseases have emerged as a significant global health issue1. Pollen is a major allergen responsible for respiratory allergic diseases, second only to dust mites. The incidence of pollen-induced allergic diseases has been increasing annually, especially in the northern regions of China, where pollen allergies are the most common cause of allergic diseases, accounting for more than 50% of cases2. Artemisia vulgaris (Art v) and Ambrosia artemisiifolia (Amb a) are among the most important weed pollens, while Phleum pratense (Phl p) and Betula verrucosa (Bet v) serve as quintessential representatives of grass and tree pollen allergens, respectively, both capable of inducing allergic symptoms3,4,5.

Art v is widely distributed across the temperate climate zones of Europe, North America, and parts of Asia. Its abundant and highly allergenic pollen is a major cause of pollinosis in late summer and early autumn6. A cross-sectional study indicates that approximately 11.3% of patients with respiratory allergic diseases in China are allergic to Art v, with this figure significantly higher in the northern regions2,7 (> 50%). Amb a, belonging to the same Asteraceae family as Art v and sharing a similar flowering period, is an important allergenic pollen during the summer and autumn seasons in northern China and Korea8,9. A study has shown that at least 35% of individuals allergic to Amb a around Milan display an allergic reaction to Art v during skin prick tests (SPT)10. Phl p releases vast amounts of pollen during the summer, making it a common allergenic grass pollen in temperate and subtropical regions11. Bet v pollen, generally peaking in April and May, is the primary tree pollen allergen in northern China12. Studies have shown that the sensitization rate of Bet v pollen in northwestern China reaches 24.2%2. Clinically, it is common to see sensitization to several types of pollen simultaneously. However, due to the seasonal overlap and cross-reactivity among different pollen species, it is challenging for clinicians to diagnose and treat individuals with multiple pollen allergies accurately. Although the major allergens of most pollens have been identified, the cross-reactivity between different pollens remains unclear.

With the advancement of recombinant technology, component-resolved diagnosis (CRD) is becoming a promising approach in allergy diagnostics. Unlike traditional methods that rely on natural allergen extracts, CRD uses purified natural or recombinant allergen proteins to identify individual sensitizing components in patients. This study employs CRD to simultaneously measure the specific IgE (sIgE) levels to Art v and its components (Art v 1), Phl p and its components (Phl p 1, Phl p 4, Phl p 5, Phl p 6, Phl p 7, Phl p 12), Bet v and its components (Bet v 1, Bet v 2), Amb a and its component (Amb a 1), and Amb p in the serum of 52 patients. The aim is to determine the sensitization patterns and correlations among pollen allergens and their components in patients with respiratory allergic diseases. Furthermore, sIgE inhibition assays were conducted on Art v, Phl p, and Bet v to analyze cross-reactivity among these pollens, providing guidance for clinical diagnosis and the selection of appropriate allergen immunotherapy (AIT) for patients with multiple pollen allergies.

The samples for this research were sourced from a large-scale, multi-center epidemiological survey project previously conducted by our team. This multi-center epidemiological survey on allergic diseases was led by the First Affiliated Hospital of Guangzhou Medical University, with participation from 25 institutions nationwide, spanning from October 2020 to January 2023. It covered seven geographical regions of China: North China, Northeast China, East China, South China, Central China, Northwest China, and Southwest China13,14. From this survey project, we selected samples from the Northwestern region for this study. Inclusion criteria included: (1) diagnosis of allergic rhinitis with or without asthma by an experienced clinician; (2) positive test for mugwort, birch, Timothy grass, or ragweed with specific IgE (sIgE ≥ 0.35 kU/L) using the ALLEOS 2000 system (Hycor Biomedical, Changsha, China); (3) no age or gender restrictions. The diagnosis of asthma and rhinitis was based on the Global Initiative for Asthma (GINA) guidelines15 and the Allergic Rhinitis and its Impact on Asthma (ARIA)16 guidelines, respectively. The exclusion criteria were as follows: (1) acute upper respiratory tract infection, systemic or other allergic, inflammatory or infectious diseases within 1 month prior to the study; (2) those with concomitant malignancies; (3) those with severe immune system disorders (including autoimmune disorders and immunodeficiency diseases, etc.); (4) cardiovascular disorders and hepatic or renal insufficiency; and (5) those with a history of specific allergen immunotherapy (6) the use of concomitant medications (e.g., antihistamines, corticosteroids, biologics) that could affect AR symptoms within one month prior to the blood collection.

The study was approved by the Ethics Committee of the First Hospital of Guangzhou Medical University (GYFYY-2020-93). All subjects were signed an informed consent form by themselves or their guardians.

Venous blood was drawn from each subject into one yellow-tipped tube (5 mL) containing procoagulant. After the tube was left to stand for 1 h at room temperature, it was centrifuged at 1000 x g for 10 min. The upper layer of serum samples was aspirated, divided into freezing tubes (500 µL per tube), and stored in a freezer at – 80 °C for uniform detection of the allergen sIgE, avoiding repeated freezing and thawing.

The allergen-specific IgE detection in this study was performed using the ALLEOS 2000TM allergen detection system by Hycor, strictly following the manufacturer’s standards. The detection system uses fluorescent magnetic particle chemiluminescence immunoassay technology, which is based on the principle that horseradish peroxidase (HRP) labels anti-human IgE antibody. This labeled anti-human IgE antibody reacts with biotinylated antigen and streptavidin-coated magnetic beads, and forms an immune complex through the antigen-antibody reaction and the streptavidin-biotin system. The immune complex reacts with the substrate and produces a luminescent signal, the intensity of which is directly proportional to the concentration of specific IgE in the serum sample17. This study measured sIgE concentrations for mugwort and its component Art v 1, birch and its components Bet v 1, Bet v 2, timothy grass and its components Phl p 1, Phl p 4, Phl p 5, Phl p 6, Phl p 7, Phl p 12, common and western ragweed and their component Amb a 1.

SIgE antibody levels were expressed in standardized units of kUA/L, with a detection range of 0.10 to 100.00 kUA/L. Tests with sIgE levels below 0.35 kUA/L were defined as negative (level 0), and those ≥ 0.35 kUA/L as positive. The sIgE results were classified into levels 1 to 6: Level 1 (0.35 to 0.70 kUA/L), Level 2 (0.70 to 3.50 kUA/L), Level 3 (3.50 to 17.50 kUA/L); Level 4 (17.50 to 50.00 kUA/L); Level 5 (50.00 to 100.00 kUA/L); Level 6 (≥ 100.00 kUA/L).

Natural or recombinant allergens for inhibition assays were purchased from INDOOR Biotechnologies Inc. (USA). Mugwort, timothy grass and birch were diluted to 100 \(\:{\upmu\:}\)g/ml, 200 \(\:{\upmu\:}\)g/ml and 200 \(\:{\upmu\:}\)g/ml respectively as inhibitor solutions. PBS was used as the blank control to determine the sIgE levels before inhibition. The serum to be tested was added to the inhibitor solution and Phosphate buffered solution (PBS) in a 1:1 ratio, mixed thoroughly, and incubated in an oven at 37 °C for 2 h for the inhibition assay, followed by sIgE detecting for the relevant allergens using the ALLEOS 2000 system. The sIgE concentrations of mugwort, timothy grass, and their component Phl p 12, as well as birch and its component Bet v 2, were measured post-incubation with the inhibitor/PBS solution.

The inhibition rate was calculated as follows: % Inhibition = (serum pre-incubated with PBS-serum pre-incubated with inhibitor)/serum pre-incubated with PBS) × 100%.

Laboratory test results were uniformly collated using Excel 2019 (Microsoft® Excel®2019) for data integration and GraphPad Prism 8.0.2 (© 1992–2019 GraphPad Software, Inc.), R Studio 2022.07.2 Build 576 (© 2009–2022 RStudio, PBC) for data analysis; and Adobe Illustrator CC 2015.0.0 (Adobe Inc.) for image integration. Categorical data were presented as frequencies (percentages), and differences between groups were compared using the Chi-square test (χ2) (Fisher’s exact test was used when theoretical frequencies were < 5), with post-hoc pairwise comparisons adjusted for significance level using the Bonferroni method. Normally distributed continuous data were expressed as mean ± standard deviation, and non-normally distributed continuous data as median (interquartile range), with differences between two groups analyzed using the t-test or Mann-Whitney U test and differences among multiple groups using one-way ANOVA or Kruskal-Wallis H test. All P values were based on two-sided tests and were considered statistically significant at P < 0.05.

A total of 52 patients were enrolled in the study, of which 34 (63.6%) were male and 18 (36.4%) were female, with an age distribution of 11 (7, 24.5) years.19 patients were diagnosed with allergic rhinitis alone, and 33 patients were diagnosed with allergic rhinitis combined with asthma. Most of the patients in the rhinitis alone and rhinitis combined with asthma groups were Han ethnicity, born by natural delivery, resided in urban areas, lived in buildings < 9 floors, used mattresses, seldom observed cockroaches at home, and did not use air conditioning (Table 1).

In the patients included in this study, the sensitization rates to Art v and its component Art v1 were 92.3% and 59.6%, respectively; Phl p sensitization was 76.9%, with the highest sensitization rate to its component Phl p 12 (63.5%), followed by Phl p 1 (25.0%); Bet v positive rate was 78.9%, with sensitization rates to its components Bet v 1 and Bet v 2 being 26.9% and 63.5%, respectively; Amb a and its component Amb a 1 had sensitization rates of 73.1% and 17.3%, respectively, while Amb p sensitization rate was 59.6% (Fig. 1A). Further analyses showed that 64.6% of Art v positive patients exhibited Art v 1 positivity (Fig. 1B); 75.0% of Phl p positive patients exhibited Phl p 12 positivity, with lower positivity rates for the other components (7.5–32.5%) (Fig. 1C); and 75.6% of Bet v positive patients exhibited Bet v 2 positivity (Fig. 1D); 23.7% of Amb a positive patients were Amb a 1 positive, whereas a comparable percentage of Amb p positive patients were Amb a 1 positive (29.0%) (Fig. 1E).

SIgE sensitization patterns of pollen crude extracts and fractions. (A) Distribution of pollen crude extracts and fractions positivity rates. (B) Sensitization between component of Art v and Art v. (C) Sensitization between components of Phl p and Phl p. (D) Sensitization between components of Bet v and Bet v. (E) Sensitization of components of Amb a and and both Amb a and Amb p. Art v Artemisia vulgaris, Phl p Phleum pretense, Bet v Betula verrucosa, Amb a Ambrosia artemisiifolia, Amb p Ambrosia psilostachya.

Spearman correlation analysis and hierarchical clustering analysis were performed on the allergen extracts and components detected. Correlation analysis based on sIgE levels showed Bet v 2 and Phl p 12 had the highest positive correlation (r = 0.98, P < 0.05). Further a strong positive correlation (0.64 ≤ r ≤ 0.80, P < 0.05) could be observed between the allergens Art v 1, Art v, Amb p, Amb a, Phl p, Phl p 12, Bet v and Bet v 12 (Fig. 2A). On the other hand, hierarchical clustering analysis based on sIgE levels categorized the 15 allergens into four sensitization categories (Fig. 2B). The first category included Amb p, Amb a, and Art v 1; the second category included Bet v 2, Phl p, Phl p 12, and Bet v; Art v was categorized on its own as the third category; and the fourth category comprised Phl p 6, Phl p 2, Phl p 7, Amb a 1, Phl p 5, Phl p 1, and Bet v 1.

(A) Spearman’s rho correlation analysis between pollen crude extract and components. (B) Hierarchical clustering analysis. Art v Artemisia vulgaris, Phl p Phleum pretense, Bet v Betula verrucosa, Amb a Ambrosia artemisiifolia, Amb p Ambrosia psilostachya.

Based on the results of cluster analysis and correlation analysis, UpSet was further used to analysis the co-sensitization between the allergens Art v and its component Art v 1, Bet v and its component Bet v 2, Amb a, Amb p, Phl p and its component Plp h 12. The highest proportion of concomitant sensitization was observed among Art v and its component Art v 1, Bet v and its component Bet v 2, Amb a, Amb p, Phl p, and its component Plp h 12 (25%) (Fig. 3). Moreover, there was evident cross-overlap among these pollens and components, with the proportion of any two or more simultaneous positives reaching up to 92.3%.

UpSet plot depicting co-sensitisation between pollen crude extract and components. Art v Artemisia vulgaris, Phl p Phleum pretense, Bet v Betula verrucosa, Amb a Ambrosia artemisiifolia, Amb p Ambrosia psilostachya. Each plot consists of three subplots, an intersection-size bar chart (top), a set-size bar chart (bottom left), and an intersection matrix between sets (bottom right). The columns of the matrix represent each intersection combination and correspond to the horizontal coordinates of the bar chart; the rows of the matrix represent the sets and correspond to the vertical coordinates of the bar chart.

In addition, we divided the patients into groups according to whether the above pollen crude extract allergens were sensitizing or not, and analyzed the sensitization rates of other crude extracts and components (Table 2). The results showed that in the Art v positive group, the sensitization rates of Phl p 12, Bet v 2, Amb a, and Amb p ranged from 64.6 to 79.2%, whereas in the Art v negative group, none of these allergens were detected positive (positivity rate of 0%), with the difference being statistically significant (all P < 0.01). Similar results were observed for the Phl p allergen, with the sensitization rates of Phl p 12, Bet v 2, Amb a, and Amb p being significantly higher in the Phl p positive group compared to the Phl p negative group (OR: 4.15 ~ 9.00). Furthermore, in the Bet v positive samples, the positivity rates for Phl p 12 and Bet v 2 were both 75.6%, compared to 18.2% in the negative group, showing a statistically significant difference (P < 0.01). In the results we also observed a higher sensitization rate for both Phl p and its components Phl p 12, Bet v 12 and Amb p in Amb a positive patients as well (all OR > 10, P < 0.01).

Based on the results of the correlation and hierarchical cluster analyses described above, there is a potential cross-reactivity between Art v, Phl p and Bet v allergens. And to test this hypothesis, we further conducted sIgE inhibition assay using crude extracts of Art v, Phl p and Bet v as inhibitors (Fig. 4; Table 3). The sIgE inhibition assay results showed that the self-inhibition rates of Art v, Phl p and Bet v were 85.60%, 79.20% and 40.00%, respectively. Art v extract exhibited an inhibition rate greater than 73.2% against Phl p and its component Phl p 12, as well as Bet v and its component Bet v 2, while Phl p extract showed inhibition rates of 80.70–89.87% against Phl p 12, Bet v and Bet v 2. Whereas, Bet v extract had inhibition rates of 21.9 to 59.8% against Phl p and Bet v 2, with a notably higher inhibition rate of 76.80% against Phl p 12. Notably, the inhibition rates of Art v by Phl p extract and Bet v extract were only 10.1% and 11.9%, respectively.

sIgE inhibition by (A) Art v, (B) Phl p and (C) Bet v protein extract. Art v Artemisia vulgaris, Phl p Phleum pretense, Bet v Betula verrucosa, Amb a Ambrosia artemisiifolia, Amb p Ambrosia psilostachya.

In this study, a CRD approach was applied to measure IgE to various pollen crude extracts and their components in patients with respiratory allergic diseases from the Northwest region of China and analyzed the cross-reactivity of three common pollens: Art v, Phl p, and Bet v, through sIgE inhibition assays. It is expected to provide new insights for patients with multiple pollen sensitization and to provide clinical advice in the diagnostic and therapeutic practice of allergies. Among the 52 pollen-sensitized patients with allergic rhinitis and or asthma included in this study, the sensitization rate of Art v allergen exceeded 90%, making it the most significant pollen allergen, followed by Phl p and Bet v. There is a significant variability in the distribution of vegetation and climatic environments in different regions, which leads to significant differences in the characteristics of pollen sensitization of allergic populations18,19. Based on CRD results, more than half of the Art v sensitized patients were positive for Art v 1, suggesting that Art v 1 is a major component of Art v, which is in line with the results of a previous study by our team20.

Profilin is a ubiquitous actin-binding protein in eukaryotes and commonly found as a cross-reactive allergen in plant pollen and plant-derived foods21. In Central Europe, sensitization to profilin has been reported to be less than 15% in allergic rhinitis patients with Bet v sensitization22. However, in our results, more than 75% of Bet v sensitized patients were sensitized to component Bet v 2 and 75% of Phl p sensitized patients were sensitized to component Phl p 12. Additionally, the results of correlation and cluster analyses suggested a significant correlation between Bet v 2 and Phl p 12. The fact that Bet v 2 and Phl p 12 belong to the same class of Profilin suggests that Profilin sensitization is common in pollen-allergic patients in north-west China, which may also explain the significant correlation between Phl p and Bet v allergens. Furthermore, previous studies have shown that over 95% of Amb a-sensitized patients exhibit Amb a 1 IgE23. However, in our study, only 23.7% and 29% of patients sensitized to Amb a and Amb p, respectively, were positive for component Amb a 1, and all of them were concomitantly sensitized to Art v. The report by Asero R et al. pointed out the cross-reactivity of Amb a, Amb a p with Art v allergens due to the high homology between Amb a 1 and Art v 1, Art v 624. A strong positive correlation between Art v and the two ragweeds was also observed in our results and was as high as 60% positive for Amb a/p in Art v positive patients compared to 0% in Art v negative groups. This further indicates the cross-reactivity between Amb a and Art v.

To further verify the cross-reactivity between the pollens, sIgE inhibition assays were conducted. It was observed that when Art v inhibitors were incubated with sera containing sIgE specific to Art v, Phl p and its component Phl p 12, and Bet v and its component Bet v 2, Art v showed a high degree of inhibition, with the inhibition rate exceeding 70% in all cases. This suggests that there is a significant cross-reactivity between Art v and Bet v and Phl p. Conversely, the inhibition rates of Phl p and Bet v inhibitors on Art v sIgE were only 10.1% and 11.9%. This may be because 64.6% of Art v positive patients were sensitized to the genuine sensitizing component Art v 1, while Bet v and Phl p positive patients had lower sensitization rates to their main sensitizing components but higher rates to cross-components Bet v 2 and Phl p 12. Therefore, the present study population was genuinely sensitized to Art v, whereas the positivity of Phl p and Bet v was due to cross-reactivity from Art v sensitization. Moreover, the inhibition rate of Phl p to Bet v component Bet v 2 and the inhibition rate of Bet v to Phl p component Phl p 12 were both over 76.8%. Of note, this study used crude extracts as inhibitors, which are not pure, and the exact allergen content within them is unknown. Crude extracts may contain multiple allergenic components at varying concentrations, which could be the reason why the self-inhibition rates do not reach 100%. And we observed poor self-inhibition by Bet v, possibly because the Bet v inhibitor raw material we used was not the same as the Bet v raw material used for detection of sIgE, which implies that there may be differences in the protein composition and allergenic epitopes of the two. Given the extremely high binding specificity of IgE antibodies, even minor epitope differences may result in a significant inhibition effectiveness. The profilin family has highly conserved amino acid sequences, and about 80% of the amino acid sequences of profilin from different sources of plants are identical, inducing the production of IgE cross-reactivity25. Components Art v 4, Phl p component Phl p 12, and Bet v component Bet v 2 all belong to Profilin, and there is a high cross-reactivity among the three26, which is consistent with the results of our inhibition assays results. Studies indicate that the first step in administering AIT for patients sensitized to multiple pollens is to distinguish between cross-sensitization (especially profilins and polcalcins) and co-sensitization. Prescribing AIT solely based on SPT or sIgE test results can lead to suboptimal therapeutic outcomes27.

This study has certain limitations that should be acknowledged. Firstly, due to the small sample size, we did not segregate participants based on the presence or absence of asthma in our sIgE inhibition experiments. This limitation may impact the generalizability of our findings, as the immune responses in asthmatic and non-asthmatic individuals may differ. A larger cohort would be necessary to validate our results and ensure they are representative of the broader population. Secondly, our study did not investigate a wider range of components for Art v and Amb a, nor did it conduct cross-inhibition assays for these additional components. This study requires further exploration to confirm cross-reactivity among their profilin components. Additionally, due to limited sample availability, we were unable to perform replicate experiments, which may affect the robustness of the results. Expanding the scope of allergenic components tested and including more comprehensive cross-inhibition assays would provide a deeper understanding of the molecular interactions driving these allergic responses. This could lead to improved diagnostic precision and the development of more effective treatment strategies for individuals with polysensitization to different pollen allergens.

In summary, Art v 1 is the major component of Art v, and the Profilin proteins of Phl p and Bet v (Phl p 12 and Bet v 2) are potential cross-reactive components that cause multiple pollen sensitization in respiratory allergy patients from northwestern China and contribute to the co-sensitization of pollen allergens such as Art v, Phl p, Bet v and Amb a.

The datasets used and/or analysed during the current study available from the corresponding author on reasonable request.

Allergen immunotherapy

Ambrosia artemisiifolia

Ambrosia psilostachya

Allergic rhinitis

Artemisia vulgaris

Allergic asthma

Betula verrucosa

Component-resolved diagnosis

Phosphate buffered solution

Phleum pratense

Specific immunoglobulin E

Skin prick test

Tetramethylbenzidine

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This study was supported by Guangzhou Science and Technology Foundation (2023A03J0365), Guangdong Zhong Nanshan Medical Foundation (20220011, 20220081).

Aoli Li and Zhifeng Huang contributed equally to this work.

Department of Clinical Laboratory, National Center for Respiratory Medicine, National Clinical Research Center for Respiratory Disease, State Key Laboratory of Respiratory Disease, Guangzhou Institute of Respiratory Health, The First Affiliated Hospital of Guangzhou Medical University, No. 28 Qiaozhong road, Liwan district, Guangzhou (Canton), 510120, China

Aoli Li, Zhifeng Huang, Qingyuan Ye, Xianhui Zheng, Jiale Zhang, Tong Chen, Wenting Luo & Baoqing Sun

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All authors contributed to the study conception and design. Material preparation and data collection were performed by performed by Qingyuan Ye and Tong Chen. Analysis were performed by Zhifeng Huang, Aoli Li, Xianhui Zheng, and Jiale Zhang. The first draft of the manuscript was written by Zhifeng Huang, Aoli Li, Wenting Luo, Baoqing Sun and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

Correspondence to Wenting Luo or Baoqing Sun.

The authors declare no competing interests.

The study was conducted in accordance with the Declaration of Helsinki, and approved by the Ethics Committee of the First Affiliated Hospital of Guangzhou Medical University (GYFYY-2020-93). All subjects were signed an informed consent form by themselves or their guardians.

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Li, A., Huang, Z., Ye, Q. et al. Profile of cross-reactivity to common pollen allergens in Northwest China based on component resolved diagnosis. Sci Rep 14, 24446 (2024). https://doi.org/10.1038/s41598-024-73465-x

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Received: 19 February 2024

Accepted: 17 September 2024

Published: 18 October 2024

DOI: https://doi.org/10.1038/s41598-024-73465-x

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