Abstract
The most important peach fruit allergen is Pru p 3, followed by Pru p 1, Pru p 4, and Pru p 7. We aimed to assess their role in subjects with peach fruit-induced allergy (anaphylaxis and OAS) and compare skin prick tests (SPT) vs. specific immunoglobulin E (sIgE) for predicting anaphylaxis. We also selected a control group. SPT included prevalent inhalant and plant food allergens plus peach peel extract. The sIgE to Pru p 1, Pru p 3, Pru p 4, and Pru p 7 were quantified. Compared with controls (n = 42), cases (n = 41) were younger (P = 0.003), more frequently female (P < 0.05) and had higher SPT positivity to peach peel (44% vs. 2.4%, P < 0.0001). There were significant differences in sensitization to several pollens: Olea europaea, Artemisia vulgaris, Prunus persica, Platanus acerifolia (all P < 0.001); and fruits: apple (P < 0.04), peanut (P < 0.002), tomato (P < 0.005), and melon (P < 0.05). Pru p 3 sIgE was detected in 61% of all cases (85% anaphylaxis and 38% OAS; P < 0.01 each) and 5% of controls (P < 0.001). Pru p 4 sIgE was present in 19% of cases and 7% of controls. The sIgE to Pru p 1 and Pru p 7 were not found. The odds ratio to predict anaphylaxis for peach peel SPT was 113 (confidence interval [CI], 20–613; P < 0.0001); for sIgE to Pru p 3, 22 (CI, 5.3–93; P < 0.0001); and for SPT positivity to selected plant food allergens, 5 (CI, 1–19; P < 0.05). In our study group, SPT with peel peach extract was a better predictor of anaphylaxis than Pru p 3 sIgE or other variables considered. The role of sIgE to Pru p 1, Pru p 4, and Pru p 7 seemed negligible.
Keywords: Peach, fruit, pollen, food hypersensitivity, allergy, anaphylaxis, skin tests, immunoglobulin E
INTRODUCTION
The high global consumption of peach fruit is made possible by large expanses of peach orchards around the world.1 In many regions, peach is also a leading cause of food allergy.2 After being reported in Mediterranean countries,2,3 studies from other European countries,4 and elsewhere have found similar results. Peach allergy can arise from primary sensitization2,3 or secondary sensitization5,6 to other plant allergens.
Pru p 3, a 10-kDa non-specific lipid transfer protein 1, is the most common allergen involved in peach fruit allergy,2,3,4 and the best marker of severity in patients sensitized to it.2,7 However, it is not the only allergen associated with allergic reactions.5,6 Like Bet v 1 from birch pollen, Pru p 1 is an 18-kDa pathogenesis-related protein and causes allergic reactions in individuals suffering from peach allergy.8 Pru p 2 is a 25 to 28-kDa thaumatin-like protein proposed as important in the Mediterranean area,9 while Pru p 4 is a 14-kDa protein in the profilins family associated with oral allergy syndrome (OAS).10 Pru p 7 is a gibberellin-regulated protein (7 kDa), associated with anaphylaxis in people negative to Pru p 3.11 Other allergens like Pru p 9 are involved in respiratory allergy.12
We studied patients who developed allergic reactions to peach fruit, with a particular focus on peach-induced anaphylaxis, in a region of high peach fruit exposure. We aimed to assess the role of the molecular components Pru p 1, Pru p 3, Pru p 4, and Pru p 7, and compare skin prick test (SPT) with peach peel extract vs. serum specific immunoglobulin E (sIgE) for predicting anaphylaxis.
MATERIALS AND METHODS
Study subjects
This study took place in Valle de Ricote: Hoya del Campo, San Jose Artesano, Ricote and Abaran villages (Murcia, South-East Spain), a region with extensive peach orchards and a population with high exposure to peach tree fruit and pollen.12,13
Subjects aged ≥ 20 years with repeated episodes of peach allergy were included. OAS was defined as previously described.2,3 When symptoms extended to 2 or more organs, we considered the reaction anaphylaxis.14 Criteria for diagnosing rhinitis, asthma and conjunctivitis were made as previously described.15
Controls aged ≥ 20 years from the same population were included. They had good tolerance to peach fruit but could be sensitized to the environmental allergens of the area. These were randomly selected from a large database of 1,000 subjects already available from a large population study. Controls were randomly taken 1 out of 24 tolerant subjects with a total number equivalent to that of the positive cases.
SPT
Participants underwent SPT for a large panel of inhalant and plant food allergens (Supplementary Data S1) provided by Inmunotek® (Madrid, Spain). Peach peel was extracted, and results evaluated as previously described.12,16 The optimal concentration for Pru p 3 in the peach extract for skin testing was determined by titration with the following concentrations of native Pru p 3: 40, 20, 15, 10, and 1 µg/mL-1 (provided by Dr. Díaz Perales, Polytechnic University, Madrid, Spain) in a group of 10 subjects with SPT positive to peach peel extract. Positive SPT was considered when the wheal area was ≥3 mm, providing that the diluent skin response was negative.
sIgE
The sIgE to Pru p 3, Pru p 4, Pru p 1, and Pru p 7 was measured by ImmunoCAP® (Thermo Fisher Scientific, Wahtham, MA, USA). Values > 0.35 kUA/L were considered positive.
Data analysis
We compared cases of allergy to peach fruit (anaphylaxis and OAS) with controls and also anaphylaxis vs. OAS.
Quantitative variables were described using means, medians, standard deviations (SDs), and confidence intervals (CIs). Qualitative variables, expressed as relative frequencies and percentages, were analyzed using the chi-squared statistic or Fisher's exact test when frequencies numbered 5 or less (Supplementary Data S2).
We also performed multivariable logistic regression using the Stepwise method for 2 different outcomes: peach-peel SPT and Pru p 3 sIgE for inducing anaphylaxis. Both models included all the study variables in the analysis. The level of significance was 0.05 and we used the SAS v 9.4 Software (SAS Institute, Cary, NC, USA).
Ethics statement
The study was approved by our Institutional Ethics Committee: Comité de ética de la investigación. Hospital General Universitario Gregorio Marañón (approval number: 41/18) and Comisión de ética investigación del Hospital Universitario Infanta Leonor y Hospital Virgen de la Torre (approval number: 100/20). All patients signed a written informed consent prior to the inclusion in the study.
RESULTS
Study subjects
We included 41 cases and 42 controls, the former were younger (median age, 35.5 years [SD, 12] vs. 44.6 years [SD, 15]; P = 0.003) and more frequently female (71% vs. 50%; P < 0.05).
The optimal concentration for Pru p 3 in the peach extract for skin testing was 20 µg/mL, which was used for our experiments.
Among the cases, 20 had anaphylaxis (Table 1) and 21 OAS (Table 2). Nearly half (44%) had a positive response to peach peel extract. Anaphylaxis was considered to be of grade 1 severity in 8 participants, grade 2 in 6, and grade 3 in 6.14
Table 1. Cases of anaphylaxis induced by peach fruit.
| Case | Age (yr) | Sex | Symptoms | SPT peach peel | Plant foods with symptoms |
|---|---|---|---|---|---|
| 1 | 22 | Male | Urticaria, systemic pruritus, and difficulty breathing with peanut and peach | + | 2 |
| 2 | 44 | Male | Systemic pruritus, lip angioedema and difficulty breathing with peach, peanut, and almond | + | 3 |
| 3 | 28 | Female | Lip angioedema, oral pruritus and difficulty breathing with peach, cherry, prune, and mango | + | 4 |
| 4 | 26 | Female | Nausea, vomiting, and systemic pruritus with peach and pomegranate | + | 2 |
| 5 | 39 | Female | Facial angioedema, Dyspnea, systemic pruritus, and abdominal pain with peach and apple. Rhinitis and difficulty breathing around peach tree orchards | + | 2 |
| 6 | 34 | Female | Generalized angioedema, systemic pruritus, and difficulty breathing with walnut. Gastrointestinal pain and eye angioedema with peach, nectarine, and apricot | + | 4 |
| 7 | 48 | Male | Systemic pruritus, nausea, vomiting, dizziness, and hypotension with banana and peach | + | 2 |
| 8 | 62 | Female | Dyspnea, facial angioedema and systemic pruritus with peach, sunflower seed and strawberry | − | 3 |
| 9 | 25 | Female | Dyspnea, generalized urticaria and difficulty breathing with peach, peanut, almond, walnut and sunflower seed | + | 5 |
| 10 | 44 | Female | Systemic pruritus, facial angioedema, and dyspnea with apricot and peanut | + | 2 |
| 11 | 33 | Female | Dyspnea, systemic pruritus and angioedema and hypotension with banana, peach, peanut and walnut | + | 4 |
| 12 | 66 | Female | Systemic pruritus and difficulty breathing with peanut, peach and apple | + | 3 |
| 13 | 23 | Female | Hypotension, generalized urticaria, and systemic pruritus with walnut and peach | + | 2 |
| 14 | 42 | Male | Oral pruritus and difficulty breathing with walnut, apple, and peach | + | 3 |
| 15 | 37 | Male | Difficulty swallowing, dysphonia, and systemic pruritus with peach, peanut, sunflower seed, almond, and pistachio | + | 5 |
| 16 | 47 | Female | Nausea, vomiting, and systemic pruritus with peach. Lip angioedema with walnut | − | 2 |
| 17 | 25 | Female | Generalized urticaria with facial angioedema and difficulty breathing with apple and peach | − | 2 |
| 18 | 35 | Female | Systemic pruritus, facial angioedema, and difficulty breathing with peanut. Oral and ear pruritus with peach | + | 2 |
| 19 | 42 | Female | Systemic pruritus, difficulty breathing, and abdominal pain with peach, peanut, and apple | + | 3 |
| 20 | 35 | Male | Facial angioedema with pruritus and abdominal pain with peach and peanut | − | 2 |
SPT, skin prick test.
Table 2. Cases of peach fruit-induced oral allergy syndrome.
| Case | Age (yr) | Sex | Symptoms | SPT peach peel | Plant foods with symptoms |
|---|---|---|---|---|---|
| 21 | 26 | Male | Facial erythema and tongue pruritus with peach, apple, pineapple, and melon | − | 4 |
| 22 | 27 | Female | Oral pruritus with peach, banana, almond, and peanut | − | 4 |
| 23 | 28 | Female | Tongue and pharyngeal pruritus with peach, melon, watermelon, and banana | − | 4 |
| 24 | 41 | Female | Tongue pruritus and lip pruritus and angioedema with peach, and peanut | − | 2 |
| 25 | 43 | Female | Oral pruritus with peach, melon, and peanut. Rhynorrhea and nose pruritus with sunflower seed | + | 4 |
| 26 | 24 | Female | Oral pruritus with peach and peanut | + | 2 |
| 27 | 32 | Female | Oral pruritus and facial erythema with peach, apricot, apple, and pear | − | 5 |
| Difficulty swallowing with pineapple | |||||
| 28 | 37 | Female | Oral and lip angioedema with peach | − | 1 |
| 29 | 39 | Female | Tongue angioedema and oral pruritus with walnut and peach | − | 2 |
| 30 | 34 | Male | Oral pruritus with peach | − | 1 |
| 31 | 29 | Female | Oral and lip angioedema with peach | − | 1 |
| 32 | 48 | Male | Tongue pruritus and angioedema with tomato, melon, peach, and apricot | − | 4 |
| 33 | 32 | Female | Pharyngeal pruritus with peach | − | 1 |
| 34 | 49 | Female | Pharyngeal pruritus and difficulty swallowing with peach and apricot | − | 2 |
| 35 | 24 | Female | Lip angioedema and tongue pruritus with melon and peach | − | 2 |
| 36 | 33 | Female | Pharyngeal pruritus with peach | − | 1 |
| 37 | 20 | Male | Lip angioedema and tongue pruritus with pineapple, melon, and peach | − | 3 |
| 38 | 33 | Female | Oral pruritus with peach | − | 1 |
| 39 | 22 | Female | Pharyngeal pruritus with peanut, walnut, peach, banana, and kiwi | − | 5 |
| 40 | 36 | Male | Tongue pruritus with peach | − | 1 |
| 41 | 62 | Male | Oral pruritus and lip angioedema with peach | − | 1 |
SPT, skin prick test.
Only 1 in the control group was positive to peach peel extract on SPT, indicating a specificity of 97.6%. This was control 20 who had also positive SPT to apple, peanut, and walnut (Supplementary Tables S1 and S2).
SPT to pollens
Although the prevalence was high with all the pollens tested in cases, the strongest association was for Olea europaea, Artemisia vulgaris, Prunus persica, and Platanus acerifolia (P < 0.001, Fig. 1). When we considered the percentage of subjects sensitized to pollens, we observed a strong statistical difference between cases and controls: 83% vs. 45% respectively (P < 0.0001) (Supplementary Table S3).
Fig. 1. Percentage of subjects with positive SPT to pollens in cases vs. controls.
NS, not significant; SPT, skin prick test.
Concurrent allergic diseases
Differences were found in cases compared with controls in conjunctivitis (76% vs. 45%, P = 0.005), rhinitis (85% vs. 50%, P = 0.001) and asthma (39% vs. 12%, P = 0.004) (Fig. 2).
Fig. 2. Concurrent allergic diseases in cases vs. controls.
SPT to plant food allergens
Differences in positivity between cases and controls were found for apple (15% vs. 2%, P = 0.04), peanut (27% vs. 2%, P = 0.002), tomato (17% vs. 0%, P < 0.005) and melon (15% vs. 2.4%, P = 0.04). SPT to plant food allergens was also higher in the cases compared with the controls (36% vs. 9.5%; P = 0.007). Supplementary Table S4 presents SPT to plant food allergens in cases.
sIgE to Pru p 3, Pru p 4, Pru p 1, and Pru p 7
The proportion of positive sIgE to Pru p 3 was detected in 61% of cases vs. 5% of controls (P < 0.001), indicating a sensitivity of 61% and specificity of 95% for this marker. There was no correlation between sIgE to Pru p 3 and anaphylaxis severity. The sIgE to Pru p 3 and Pru p 4 were 19% and 7%, respectively, with no significant differences between the groups. This result provided a very low sensitivity, but a good specificity (93%). For Pru p 1 and Pru p 7, we did not observe any positive result (Supplementary Table S5).
Comparison of anaphylaxis vs. OAS
When comparing anaphylaxis vs. OAS, no differences were observed in age or sex (Table 3). Eighty percent of cases with anaphylaxis had a positive SPT to peach, compared with only 9.5% of cases with OAS (P < 0.001). Sensitization to pollen tended to be higher in anaphylaxis cases, except for Cupressus arizonica, but these differences were not significant. No differences were observed for conjunctivitis, rhinitis, or asthma. Sensitization to plant food allergens was also more likely in anaphylaxis cases, with significant differences for apple (25% vs. 4%, P < 0.05) and peanut (40% vs. 14%, P < 0.05) (Table 3). In consonance with these observations, 50% of anaphylaxis cases vs. 24% of OAS were sensitized to plant food allergens (P = 0.03).
Table 3. Comparison of cases of Anaphylaxis vs. OAS to peach.
| Variables | Anaphylaxis (n = 20) | Oral allergy syndrome (n = 21) | P value | |
|---|---|---|---|---|
| Age (yr) | 38 ± 12 | 33 ± 12 | NS | |
| Sex (female/total) | 48 | 52 | NS | |
| SPT + to peach peel | 80 | 9.5 | < 0.001 | |
| Positive SPT to pollen | ||||
| Phleum pratense | 55 | 33 | NS | |
| Cupressus arizonica | 15 | 24 | NS | |
| Olea europaea | 70 | 62 | NS | |
| Platanus acerifolia | 35 | 19 | NS | |
| Artemisia vulgaris | 40 | 19 | NS | |
| Prunus persica | 70 | 52 | NS | |
| Parietaria judaica | 35 | 24 | NS | |
| Salsola kali | 35 | 33 | NS | |
| NP | 90 | 76 | NS | |
| Clinical entities | ||||
| Conjunctivitis | 85 | 66 | NS | |
| Rhinitis | 90 | 81 | NS | |
| Asthma | 45 | 33 | NS | |
| Positive SPT to plant foods | ||||
| Apple | 25 | 4 | < 0.05 | |
| Banana | 5 | 0 | - | |
| Peanut | 40 | 14 | < 0.05 | |
| Almond | 10 | 14 | NS | |
| Walnut | 20 | 5 | NS | |
| Tomato | 25 | 9 | NS | |
| Kiwi | 5 | 9 | NS | |
| Melon | 15 | 14 | NS | |
| Pineapple | 0 | 0 | NS | |
| N+ | 50 | 24 | 0.03 | |
| Positive serum specific IgE to peach components | ||||
| Pru p 3 | 85 | 38 | < 0.001 | |
| Pru p 4 | 20 | 19 | NS | |
| Pru p 1 | 0 | 0 | NS | |
| Pru p 7 | 0 | 0 | NS | |
Data are shown as median ± standard deviation or number (%).
NS, not significant; SPT, skin prick test; NP, percentage of cases with positive SPT to pollen; N+, percentage of cases with positive SPT to plant foods; IgE, immunoglobulin E. Bold numbers: statistically significant.
Differences were observed in sensitivity in Pru p 3 sIgE, which were found in 85% of cases with anaphylaxis vs. 38% with OAS (P < 0.001). Pru p 4 sIgE was detected equally in both subgroups (20% vs. 19%, respectively) (Table 3).
Logistic regression analysis showed a highly significant association between a positive SPT to peach peel and anaphylaxis: odds ratio (OR), 113 (CI, 20–613; P < 0.0001). The predictive value of Pru p 3 sIgE antibodies for this outcome was substantially lower (OR, 22; CI, 5.3–93; P < 0.0001), as was sensitization to other plant food allergens (OR, 5; CI, 1–19; P < 0.05). The OR of other variables included in the analysis and described in Supplementary Data S1 or S2 did not show statistical significance.
Sensitivity and negative predictive value of peach peel SPT and Pru p 3 sIgE for anaphylaxis were similar (80% vs. 85% and 93.7% vs. 94.5%, respectively) whereas specificity and positive predictive value were higher for peach peel SPT (95.2% vs. 82.5% and 84.2% vs. 60.7%, respectively) (Supplementary Tables S6).
DISCUSSION
It is well known that allergy to fruits, including peach, is variable in different world regions and that the context in which sensitization develops is related to the intake of other fruit and plant food allergens as well as pollen inhalation.3,4,14
We tested the classic pollen and plant food allergens prevalent in the population. We included peach peel extract, as a source of Pru p 3 at 20 µg/mL, the optimal concentration for SPT. For the other allergens like Pru p 1 and Pru p 4, SPT with peach peel extract has proven inadequate due to their thermolability.3,17,18,19 Peach peel extract has also been shown to contain peamaclein, also known as Pru p 7,19 although we did not estimate the presence in our extract.
For verifying the contribution of the peach allergens, we used commercially available assay for Pru p 1, Pru p 3, Pru p 4, and Pru p 7. Although Pru p 3 is a major inducer of peach allergy, the precise extent of its contribution depends on the areas where the studies are taken. Initially reported in Mediterranean countries,2,3 the leading role has also been reported in Central Europe4 and elsewhere.5,6,11 Regarding Pru p 9, a recently recognized allergen,12,13 it is not present in fruits and therefore does not contribute to sensitization from peach intake.12
Cases were selected based on repeated episodes of allergy to peach fruit. In our study, 44% of cases were SPT positive to peach peel, but when we stratified participants in 2 groups according to clinical entity, the sensitivity was 80% in anaphylaxis and 9.5% in OAS. Thus, SPT sensitivity depends on the clinical manifestations. The fact that this value is under 100% in most studies suggests that other peach allergens may play a role in sensitization.18,19
We observed significant differences in the sensitization to O. europaea, A. vulgaris, P. persica, and P. acerifolia pollens in cases vs. controls. The high association observed for P. persica and O. europaea could be explained by the presence of a glucan endo-1,3-beta-glucosidase-like protein in peach tree pollen also present in O. europaea pollen (Ole e 4) and a P. persica pollen polygalacturonase, related to Ole e 14.12 The high response to P. acerifolia and A. vulgaris can be explained by Pru p 3 cross-reactivity with Pla a 3, and Art v 3.20,21
As for skin sensitization to different plant food allergens in our cases, a significant difference was observed with apple and peanut, 2 fruits with equivalent lipid transfer proteins (LTPs; Mal d 3 and Ara h 9).22,23 Other sources of LTPs are almond and tomato.24 Sensitization to melon could be explained by the presence of profilin, also existing in peach fruit.12,25
Our study group included a similar number of cases with anaphylaxis and OAS. The high proportion of subjects sensitized to peach in the anaphylaxis subgroup contrasted with the low number in the OAS subgroup. A plausible reason may be that labile allergens were not represented in the allergenic extract, possibly leading to an underrepresentation of cases with OAS, where LTP values are lower than with anaphylaxis.
Although it has been reported that pollen allergy is associated with OAS,14,17 in our study the number of positive cases to pollens was higher than that reported in the control group, but similar between the anaphylaxis and OAS subgroups. As for sensitization to plant food allergens, the anaphylaxis subgroup showed a much higher sensitization than the OAS subgroup to apple and peanut. This general pattern held for sensitization to other plant food allergens, but these data were difficult to interpret due to the underrepresentation of thermolabile allergens in fruit allergen extracts.18,19
Pastorello et al. 10 reported 65.8% positivity to Pru p 1 in OAS vs. 31.9% in anaphylaxis, and 40.8% positivity to Pru p 4 in OAS vs. 18.1% in anaphylaxis. In northern Italy, another group reported sensitization to Pru p 1 of 42.8% and to Pru p 4 of 12.7%, while in southern Italy no positives cases were found.26 In contrast to other studies carried out in Spain, we did not find serum specific IgE antibodies to PR-10 allergens quantified with Pru p 1.27 In line with other reports, data in our study group showed that 19% of cases were sensitized to Pru p 4 with no differences between anaphylaxis and OAS subgroups.26,27 Pru p 7 may have a role, particularly in cases of peach anaphylaxis that are negative to Pru p 3.28 However, in our study no association was found with cases positive to cypress pollen.29
Although our cases were not challenged with peach fruit, the consistent and repeated history of allergic reactions and positive skin tests strongly supported the diagnosis of peach allergy. We did not include cases with urticaria or other clinical entities because of the very low prevalence in the population evaluated. Another issue worth considering was the wide confident interval of the OR for peach peel SPT that weakened the conclusion of our study. This may have been attributed to the sample size and distribution of subjects.
Our data provided evidence for the role of skin testing with peach peel extract and commercial assays with available molecular components of peach fruit for evaluating people sensitized and with allergy to peach fruit. Results indicated that a positive skin test for peach peel extract was the strongest predictor of anaphylaxis, yielding an OR 5 times higher than sIgE antibodies to Pru p 3 and 22 times greater than a positive skin test to plant food allergens. Ongoing studies are investigating the role of other peach fruit allergens, particularly those involved in OAS.
ACKNOWLEDGMENTS
We thank Ms Meggan Harris for the English edition of the manuscript and Mr Carlos Goetz (Pertica®, Madrid, Spain) for the statistical analysis. We also thank Universidad Complutense de Madrid (Madrid, Spain) for the academic support.
This work was supported by grants PI17/00615 and PI20/00607 awarded by the Ministry of Economy and Competiveness and the Institute of Health Carlos III, and co-funded by the European Regional Development Fund (ERDF) for the Thematic Networks and Co-operative Research Centres: ARADyAL (RD16/0006/0032 and RD16/0006/0024).
Footnotes
Disclosure: There are no financial or other issues that might lead to conflict of interest.
SUPPLEMENTARY MATERIALS
The allergens tested
Variables
Skin prick test results to inhalant allergens and concurrent allergic diseases in the control group
Skin prick tests to plant foods in the control group
Skin prick test results to inhalant allergens and concurrent allergic diseases in cases
Skin prick tests to other plant foods in cases of peach allergy
Serum specific immunoglobulin E (kUA/L) to peach components in cases
Sensitivity, specificity as well as positive and negative predictive values for peach peel skin prick test and serum specific IgE to Pru p 3 for anaphylaxis
References
- 1.Food and Agriculture Organization of the United Nations. Production of peaches and nectarines in 2016 [Internet] Rome: Food and Agriculture Organization of the United Nations, Statistics Division (FAOSTAT); 2018. [cited 2018 Mar 5]. Available from: http://www.fao.org/faostat/en/#data/QC/ [Google Scholar]
- 2.Fernández-Rivas M, González-Mancebo E, Rodríguez-Pérez R, Benito C, Sánchez-Monge R, Salcedo G, et al. Clinically relevant peach allergy is related to peach lipid transfer protein, Pru p 3, in the Spanish population. J Allergy Clin Immunol. 2003;112:789–795. doi: 10.1016/S0091. [DOI] [PubMed] [Google Scholar]
- 3.Asero R, Mistrello G, Roncarolo D, Casarini M, Falagiani P. Allergy to nonspecific lipid transfer proteins in Rosaceae: a comparative study of different in vivo diagnostic methods. Ann Allergy Asthma Immunol. 2001;87:68–71. doi: 10.1016/S1081-1206(10)62326-5. [DOI] [PubMed] [Google Scholar]
- 4.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. doi: 10.1111/all.13151. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 5.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. doi: 10.1016/j.jaci.2012.07.015. [DOI] [PubMed] [Google Scholar]
- 6.Kim JH, Kim SH, Park HW, Cho SH, Chang YS. Oral allergy syndrome in birch pollen-sensitized patients from a Korean University Hospital. J Korean Med Sci. 2018;33:e218. doi: 10.3346/jkms.2018.33.e218. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 7.Gaier S, Oberhuber C, Hemmer W, Radauer C, Rigby NM, Marsh JT, et al. Pru p 3 as a marker for symptom severity for patients with peach allergy in a birch pollen environment. J Allergy Clin Immunol. 2009;124:166–167. doi: 10.1016/j.jaci.2009.02.023. [DOI] [PubMed] [Google Scholar]
- 8.Führer S, Trimmel S, Breuker K, Tollinger M. NMR resonance assignments of the pathogenesis-related peach allergen Pru p 1.0101. Biomol NMR Assign. 2019;13:127–130. doi: 10.1007/s12104-018-9864-x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 9.Palacín A, Rivas LA, Gómez-Casado C, Aguirre J, Tordesillas L, Bartra J, et al. The involvement of thaumatin-like proteins in plant food cross-reactivity: a multicenter study using a specific protein microarray. PLoS One. 2012;7:e44088. doi: 10.1371/journal.pone.0044088. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 10.Pastorello EA, Farioli L, Pravettoni V, Scibilia J, Mascheri A, Borgonovo L, et al. Pru p 3-sensitised Italian peach-allergic patients are less likely to develop severe symptoms when also presenting IgE antibodies to Pru p 1 and Pru p 4. Int Arch Allergy Immunol. 2011;156:362–372. doi: 10.1159/000324440. [DOI] [PubMed] [Google Scholar]
- 11.Ando Y, Miyamoto M, Kato M, Nakayama M, Fukuda H, Yoshihara S. Pru p 7 predicts severe reactions after ingestion of peach in Japanese children and adolescents. Int Arch Allergy Immunol. 2020;181:183–190. doi: 10.1159/000504367. [DOI] [PubMed] [Google Scholar]
- 12.Blanca M, Victorio Puche L, Garrido-Arandia M, Martin-Pedraza L, Romero Sahagún A, López-Sánchez JD, et al. Pru p 9, a new allergen eliciting respiratory symptoms in subjects sensitized to peach tree pollen. PLoS One. 2020;15:e0230010. doi: 10.1371/journal.pone.0230010. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 13.Victorio Puche L, Somoza ML, López-Sánchez JD, Garrido-Arandia M, Díaz-Perales A, Blanca M. Peach tree pollen and prunus persica 9 sensitisation and allergy in children and adolescents. Int Arch Allergy Immunol. 2019;180:212–220. doi: 10.1159/000502352. [DOI] [PubMed] [Google Scholar]
- 14.Ring J, Behrendt H, de Weck A. History and classification of anaphylaxis. Chem Immunol Allergy. 2010;95:1–11. doi: 10.1159/000315934. [DOI] [PubMed] [Google Scholar]
- 15.Johansson SG, Bieber T, Dahl R, Friedmann PS, Lanier BQ, Lockey RF, et al. Revised nomenclature for allergy for global use: report of the nomenclature review committee of the World Allergy Organization, October 2003. J Allergy Clin Immunol. 2004;113:832–836. doi: 10.1016/j.jaci.2003.12.591. [DOI] [PubMed] [Google Scholar]
- 16.Hassan AKG, Venkatesh YP. An overview of fruit allergy and the causative allergens. Eur Ann Allergy Clin Immunol. 2015;47:180–187. [PubMed] [Google Scholar]
- 17.Duffort OA, Polo F, Lombardero M, Díaz-Perales A, Sánchez-Monge R, García-Casado G, et al. Immunoassay to quantify the major peach allergen Pru p 3 in foodstuffs. Differential allergen release and stability under physiological conditions. J Agric Food Chem. 2002;50:7738–7741. doi: 10.1021/jf0258398. [DOI] [PubMed] [Google Scholar]
- 18.Carnés J, Fernández-Caldas E, Gallego MT, Ferrer A, Cuesta-Herranz J. Pru p 3 (LTP) content in peach extracts. Allergy. 2002;57:1071–1075. doi: 10.1034/j.1398-9995.2002.23732.x. [DOI] [PubMed] [Google Scholar]
- 19.Asero R, Aruanno A, Bresciani M, Brusca I, Carollo M, Cecchi L, et al. Evaluation of two commercial peach extracts for skin prick testing in the diagnosis of hypersensitivity to lipid transfer protein. A multicenter study. Eur Ann Allergy Clin Immunol. 2021;53:168–170. doi: 10.23822/EurAnnACI.1764-1489.144. [DOI] [PubMed] [Google Scholar]
- 20.Ruano-Zaragoza M, Somoza ML, Jiménez-Rodriguez TW, Soriano-Gomis V, González-Delgado P, Esteban-Rodriguez A, et al. Lipid transfer protein sensitization: risk of anaphylaxis and molecular sensitization profile in Pru p 3-sensitized patients. Int Arch Allergy Immunol. 2021;182:425–432. doi: 10.1159/000511977. [DOI] [PubMed] [Google Scholar]
- 21.Sánchez-López J, Tordesillas L, Pascal M, Muñoz-Cano R, Garrido M, Rueda M, et al. Role of art v 3 in pollinosis of patients allergic to Pru p 3. J Allergy Clin Immunol. 2014;133:1018–1025. doi: 10.1016/j.jaci.2013.08.005. [DOI] [PubMed] [Google Scholar]
- 22.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. doi: 10.1016/j.jaci.2006.05.012. [DOI] [PubMed] [Google Scholar]
- 23.Javaloyes G, Goikoetxea MJ, García Nuñez I, Aranda A, Sanz ML, Blanca M, et al. Pru p 3 acts as a strong sensitizer for peanut allergy in Spain. J Allergy Clin Immunol. 2012;130:1432–1434.e3. doi: 10.1016/j.jaci.2012.08.038. [DOI] [PubMed] [Google Scholar]
- 24.Martín-Pedraza L, González M, Gómez F, Blanca-López N, Garrido-Arandia M, Rodríguez R, et al. Two nonspecific lipid transfer proteins (nsLTPs) from tomato seeds are associated to severe symptoms of tomato-allergic patients. Mol Nutr Food Res. 2016;60:1172–1182. doi: 10.1002/mnfr.201500782. [DOI] [PubMed] [Google Scholar]
- 25.Santos A, Van Ree R. Profilins: mimickers of allergy or relevant allergens? Int Arch Allergy Immunol. 2011;155:191–204. doi: 10.1159/000321178. [DOI] [PubMed] [Google Scholar]
- 26.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. doi: 10.1186/s12948-015-0035-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 27.Gamboa PM, Cáceres O, Antepara I, Sánchez-Monge R, Ahrazem O, Salcedo G, et al. Two different profiles of peach allergy in the north of Spain. Allergy. 2007;62:408–414. doi: 10.1111/j.1398-9995.2006.01284.x. [DOI] [PubMed] [Google Scholar]
- 28.Tuppo L, Alessandri C, Pomponi D, Picone D, Tamburrini M, Ferrara R, et al. Peamaclein--a new peach allergenic protein: similarities, differences and misleading features compared to Pru p 3. Clin Exp Allergy. 2013;43:128–140. doi: 10.1111/cea.12028. [DOI] [PubMed] [Google Scholar]
- 29.Sénéchal H, Keykhosravi S, Couderc R, Selva MA, Shahali Y, Aizawa T, et al. Pollen/fruit syndrome: clinical relevance of the cypress pollen allergenic gibberellin-regulated protein. Allergy Asthma Immunol Res. 2019;11:143–151. doi: 10.4168/aair.2019.11.1.143. [DOI] [PMC free article] [PubMed] [Google Scholar]
Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Supplementary Materials
The allergens tested
Variables
Skin prick test results to inhalant allergens and concurrent allergic diseases in the control group
Skin prick tests to plant foods in the control group
Skin prick test results to inhalant allergens and concurrent allergic diseases in cases
Skin prick tests to other plant foods in cases of peach allergy
Serum specific immunoglobulin E (kUA/L) to peach components in cases
Sensitivity, specificity as well as positive and negative predictive values for peach peel skin prick test and serum specific IgE to Pru p 3 for anaphylaxis