Navarro et al. Allergy Asthma Clin Immunol (2019) 15:60 Allergy, Asthma & Clinical Immunology https://doi.org/10.1186/s13223-019-0374-x SHORT REPORT Open Access Oral immunotherapy with peach juice in patients allergic to LTPs Begoña Navarro1, Eladia Alarcón1, Ángela Claver1, Mariona Pascal2, Araceli Díaz‑Perales3 and Anna Cisteró‑Bahima1* Abstract Introduction: To assess the safety and efficacy of an oral immunotherapy regimen in patients with allergy to lipid transfer proteins (LTPs). Materials and methods: Prospective study of 24 patients allergic to LTP with positive skin test and a history of anaphylaxis. All patients underwent a desensitization protocol with commercial peach juice. Rising doses of peach juice were administered, starting with an initial dose of seven drops of a 1/1000 dilution and finishing with a dose of 5 ml at visit 17. At visit 18, all patients performed an open challenge with whole juice at a cumulative dose of 200 ml. All adverse reactions occurring during the administration of the different doses were recorded. Levels of rPru p 3 in the juice were quantified. Results: There were no severe reactions during the desensitization process in the 24 patients. Seven patients (29%) reported mild oral symptoms, and two patients (8%) had urticaria associated with co-factors (one due to exercise and another due to non-steroidal anti-inflammatory drugs). Nineteen patients were able to swallow 5 ml of juice and five withdrew from the study. In two pregnant patients the final challenge was not performed. In all, 17/24 patients were able to consume 200 ml peach juice without developing symptoms. Conclusions: Oral immunotherapy with the regimen used in this study is an effective and safe short-term therapeutic option for patients with allergy to LTPs. Commercial peach juice appears to be suitable for this treatment. Keywords: Anaphylaxis, Sublingual immunotherapy, Peach, Allergy Introduction maximum tolerated threshold dose [6]. The possibility Lipid transfer proteins (LTPs) are the primary cause of of inducing desensitization to peach LTPs has given rise food allergy in the adult population in the Mediterranean to several studies [7–12] in which commercial products area [1, 2]. LTPs are a family of proteins that are widely with a known quantity of this protein are developed to distributed in the plant kingdom [3], and are found in the allow the design of sublingual desensitization protocols pollen of trees, plants and latex. The fruit most widely [10, 12]. implicated in this allergy is the peach [4, 5]. After several months of sublingual immunotherapy Oral immunotherapy (OIT) to food consists of (SLIT), many patients who previously presented positive the oral administration of the food allergen causing skin tests or anaphylaxis to certain foods due to their the symptoms, starting with minimal amounts and LTP content are able to consume these foods without progressively increasing until reaching the normal adverse reactions [10]. However, since 2015, difficulties amount ingested according to the subject’s age or the in obtaining the fresh fruit required to extract the LTPs have limited the possibility of carrying out SLIT. Based on the OIT protocols for cow and egg milk *Correspondence: annacistero@gmail.com proteins developed by our group [13, 14], we describe 1 Allergy Department, Hospital Universitari Dexeus (GQS), Universitat an OIT protocol using fresh product in patients allergic Autònoma de Barcelona, Calle Sabino Arana, 5‑19, 08028 Barcelona, Spain to LTPs. Due to the difficulty of obtaining fresh peaches Full list of author information is available at the end of the article © The Author(s) 2019. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/ publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Navarro et al. Allergy Asthma Clin Immunol (2019) 15:60 Page 2 of 6 throughout the year, commercial peach juice packaged in with the involvement of more than one organ [15]. We cartons was used. The brand (Granini) uses fruit obtained excluded patients who were sensitized to LTP without from an area of Italy with a high percentage of residents symptoms, pregnant patients, patients with severe allergic to LTP. immune and/or cardiovascular diseases and/or patients receiving treatment with beta blockers. Patients with Materials and methods poor treatment compliance and patients who do not Study population understand the aim of the study were also excluded. The This prospective study carried out from January 2015 study was approved by the Center’s Ethical Committee to October 2016 included 24 patients allergic to LTP (act of approval 54/2018) and the patients provided of LTP (Bial-Aristegui®, Bilbao, Spain) and a history with a positive skin test to a 0.1 mg/ml concentration signed informed consent prior to recruitment. All patients underwent a detailed medical history, of anaphylaxis to peach (Table 1). Twenty-one (87%) including information on atopy and previous symptoms patients also presented anaphylaxis after ingesting of respiratory allergy, as well as the clinical symptoms, nuts and, in three cases, anaphylaxis reactions also causative foods, and possible cofactors involved in the occurred after the intake of lettuce, plum and/or cherry. reaction. In addition, all patients manifested minor symptoms (oral allergy syndrome, mild urticaria) after ingestion Skin tests of pneumoallergens including profilin (ALK-Abelló®, of other foods such as lettuce and rosacea fruits. The Skin tests were performed in the forearm, with a battery Madrid, Spain) and LTP (Bial-Aristegui®, Bilbao, anaphylactic reaction in all patients was Grade II or III, Spain), in addition to the foods involved in the reaction. Table 1 Demographic characteristics of the study Tests which presented wheals equal to or larger than population histamine-induced wheals were considered positive. Sex, male, n 7 Prick-by-prick tests were performed with commercial Age (mean and range), years 25.5 (5–42) peach juice at different dilutions to establish the “end Clinical symptoms (anaphylaxis) 24 (9 associated with a cofactor: 4 point”. The dilutions of the juice used to carry out the exercise and 5 NSAIDs) tests were 1/10, 1/100 and 1/1000. Skin prick tests with Specific IgE n (%) kU/La these samples were performed in order to determine the safest dilution for the patient to start the OIT regimen Pru p 3 24 (100) 7.43 (0.40–100) (end point). The starting dose in the challenge was Peach 24 (100) 6.77 (1.00–76.10) the one with a wheal area smaller than the histamine- Green bean 6 (25) 3.44 (0.44–71.00) induced wheal [16]. Almond 8 (33) 2.91 (0.41–7.57) Hazelnut 10 (42) 2.53 (0.62–16.30) Measurement of specific IgE Nut 8 (33) 16.00 (2.44–42.90) Total IgE, baseline tryptase and specific IgE to the foods Peanut 16 (67) 1.50 (0.42–22.70) involved were measured. Levels of specific IgE to Pru p 3 Lettuce 6 (25) 2.54 (0.58–20.00) LTP (Bial-Aristegui®) and the prick-by-prick test with were also quantified. The responses to the prick test with Apple 7 (29) 2.64 (0.59–32.00) Chickpea 2 (8) 11.79 (3.28–20.30) juice were recorded at each dose increase. Plum 3 (12) 3.23 (1.60–30.10) Lentil 3 (12) 1.26 (1.06–21.50) Source of the allergen Sunflower pip 3 (12) 10.70 (8.00–10.88) The source of the allergen used for the desensitization Grape 3 (12) 2.28 (0.59–3.54) protocol was a commercial peach juice (Granini, Eckes Wheal diameter prick-test LTP 7.75 (3.00–11.50) Granini Iberica SA, Barcelona) which uses the Percoca (mm)a peach variety, from Italy. The stability of rPru p 3 in the ­Granini® juice (mm)a Wheal diameter prick-by-prick 6.00 (3.50–11.00) juice was analysed by prick-by-prick test up to 1–2 weeks Prick-by-Prick ­Granini® juice 1/100 (6 patients) after the carton was opened. dilutions at end point 1/10 (14 patients) Agarose gel electrophoresis analysis of the commercial 1/1 (4 patients) peach juice was performed and the levels of rPru p 3 were Prior ALK-Abelló® peach SLIT, n (%) 7 (29%) quantified. For this quantification, 1 ml of the juice was precipitated with 10% TCA for 1 h at 4 °C. The precipitate NSAIDs nonsteroidal anti-inflammatory drugs, LTPs lipid transfer proteins, SLIT sublingual immunotherapy obtained was washed extensively with cold acetone. After a Data are expressed as median (range) drying the precipitate, it was resuspended in Phosphate Navarro et al. Allergy Asthma Clin Immunol (2019) 15:60 Page 3 of 6 buffered saline (PBS) and used to coat Enzyme-Linked unit and also daily at home, before returning to our ImmunoSorbent Assay (ELISA) plates. After blocking, unit to increase the dose after 7–15 days. From visit 8 the samples were incubated with antibody produced onwards patients began to swallow the drops, starting against Pru p 3 (1:1000) and developed with peroxidase- with one undiluted drop (1/1) until reaching a dose of tests were repeated with LTP (Bial-Aristegui®, Bilbao, bound secondary antibody. The amount of LTP contained 5 ml by visit 17. Before each dose increase, the skin in the sample was determined by extrapolation of values to that obtained by a standard curve with known values Spain), with the commercial peach juice which patients of Pru p 3. The determination was made using three returned after administration at home and with the different batches of juice, and repeated three times in new carton of juice open for the dose increases. each batch. Finally, at visit 18, all patients underwent no symptoms with the whole juice until reaching a cumulative dose Sublingual specific immunotherapy (desensitization of 200 ml. This amount was subsequently maintained protocol) at home, either daily or at least three times a week. All Table 2 shows the desensitization protocol used in the adverse reactions occurring during the administration study. The OIT was performed in four stages divided of the various doses were recorded. into 18 visits at our unit. Increasing doses of peach The final goal was for patients to ingest a serving- juice were administered, starting with an initial dose sized amount of peach, either 200 ml of peach juice of seven drops of a 1/1000 dilution until reaching a (the size of the juice box) or a serving of fresh peach. dose of 5 ml at visit 17. During the first seven visits, If for any reason this figure was not reached, oral food the dose was administered sublingually and was challenge was considered satisfactory if the patient did kept in the mouth for 2 min without being ingested. not present adverse effects with the dose reached and if Subsequently, patients maintained this dose at our the challenge with peach was well tolerated. ­ ranini® peach juice Results Table 2 OTI guidelines with G Twenty-four patients were included, aged between Stage 1. Sublingual 2 min and then spit out 5 and 42 years (seven males) and diagnosed with Visit 1 (dilution 1/1000) 1–2–4 drops anaphylaxis due to allergy to peach (Table 1) in the Visit 2 (dilution 1/100) 1–2–4 drops 3 months preceding their inclusion in the study. In nine Visit 3 (dilution 1/10) 1–2–4 drops patients, co-factors were present in the anaphylactic Visit 4 (1/1: undiluted juice) 1 drop reactions (exercise in four and use of non-steroidal anti- Visit 5 (1/1) 2 drops inflammatory drugs, NSAIDs, in five). At the time of against LTP (Bial-Aristegui®) and specific IgE to rPru p Visit 6 (1/1) 4 drops diagnosis, all the patients presented positive skin tests Visit 7 (1/1) 5 drops SLIT with a commercial extract (ALK-Abelló®, Madrid, Stage 2. Sublingual 2 min and swallow (drops) 3. Seven patients (29%) had previously undergone peach Visit 8 (1/1) 1 drop Visit 9 (1/1) 2 drops Spain) for 4 to 18 months. At the time of the study, these Visit 10 (1/1) 4 drops patients had been untreated for a period of 4–6 months. Visit 11 (1/1) 5 drops (equivalent to 0.13 ml) No differences in the initial dilution were found between Stage 3. Sublingual 2 min and swallow (ml) patients with a history of treatment with ALK peach Visit 12 0.25 ml SLIT and those without. Visit 13 0.50 ml No significant differences were found in the wheals produced by the prick-by-prick test performed either Visit 14 1 ml with the juice just opened or with the juice returned by Visit 15 2 ml the patient within 8–15 days of taking the doses at home Visit 16 3 ml (Fig. 1). Visit 17 5 ml The agarose gel electrophoresis analysis of the peach Stage 4. Oral tolerance test with whole juice juice showed a band of 10 kDa that was identified as Pru Visit 18 10–25–65–100 ml (accumulated dose 200 ml) p 3 (Fig. 2). Quantification by ELISA showed that the Continue intake of 200 ml/day (1 carton), at least 4 days/week commercial juice had an LTP concentration of 21.16 μg/ ml (Table 3). The increases were performed in a controlled manner at the immunotherapy unit every 1, 2 or every 4 weeks, depending on tolerance. Previously, prick- The desensitization pattern was started with the test to LTP and prick-by-prick test to juice were repeated (with the used and dilution of peach juice prior to the one that induced the new cartons), to assess the possible loss of protein activity of the product administered at home a wheal equal to the histamine-induced wheal (end Navarro et al. Allergy Asthma Clin Immunol (2019) 15:60 Page 4 of 6 11 10 9 Mean wheal size (mm) 8 7 6 5 4 3 2 1 0 1A 2A 3 B 4 A 5 B A B A B A B A B Visit 1 Visit 2 Visit 3 Visit 4 Visit 5 Visit 6 Visit 7 Fig. 1 Prick-by-prick test performed either with the juice just opened (a) or with the juice returned by the patient within 8-15 days of taking the doses at home (b) Table 3 Dose of Pru p 3 in peach juice vs sublingual peach kDa immunotherapy Pru p 3 Pru p 3 dose: 5 drops at maximum µg/ml concentration (µg) (5 drops = 0.13 ml) ALK juice SLIT 50 6.5 (jar 4: maximum concentration) Granini® peach juice 21.16 2.75 SLIT sublingual immunotherapy 35 (five previously treated with ALK-Abelló® peach SLIT); 14 patients started desensitization with a 1/10 dilution 25 previously treated wth ALK-Abelló® peach SLIT). From four patients started the protocol with a 1/1 dilution (one that point onwards, the doses continued to increase in accordance with the protocol (Table 2). There were no serious reactions during the desensitization process; none presented any serious reactions during 15 the process. Fifteen patients out of 24 (63%) presented no reaction of any kind, 7/24 (29%) reported mild oral symptoms, which remitted immediately with the intake of cold water, and finally 2/24 (8%) had urticaria after taking 10 the dose at home, associated with co-factors (exertion, non- steroidal anti-inflammatory drugs). As regards cutaneous reactivity, the size of the wheals 1 2 Fig. 2 Agarose gel electrophoresis with ­Granini® commercial peach in the skin tests performed with commercial peach juice decreased between visits T0 and T1 (p = 0.049), but there juice: 10 μg/2 ml precipitate with TCA 20%. 1. Coomassie staining; 2. tests with LTP (Bial-Aristegui®) in none of the intervals Anti-Pru p 3 (1:1000). A band of 10 kDa is visible in lane 2 was no reduction in the size of the wheals in the skin or between visits T0 and T2 in the commercial peach point). The desensitization regimen was initiated with juice (Fig. 3). previously been treated with ALK-Abelló® peach SLIT); the 1/100 dilution in six patients (one of whom had Desensitization was induced in 19/24 (79%) of patients. Fourteen patients were able to swallow 200 ml Navarro et al. Allergy Asthma Clin Immunol (2019) 15:60 Page 5 of 6 is possible; however, extracts are not uniformly 15 p = 0.049 accessible. The current study offers a safe and effective desensitization protocol using a widely available and Mean skin test (mm) cost-effective commercial juice, which can improve 10 patients’ access to this important therapy [8–10]. As the LTP concentration of the juice is unknown a priori, the trial simulates the situation in real life since we do not know the LTP concentration of the fruit and 5 vegetables consumed by our patients. After OIT, most of our patients were able to ingest up to 200 ml of juice after 18 visits; there are few adverse reactions, and the 0 skin reactivity to the juice is reduced. In addition, the protocol has proved to be both safe and effective: no 0) 1) 2) 0) 1) 2) (T (T (T severe reactions were recorded during the protocol and (T (T (T P P P e e e ic ic ic LT LT LT all patients presented no symptoms when swallowing the Ju Ju Ju Fig. 3 Skin test with LPT and with ­Granini® commercial peach juice: juice. T0—before stage 1; T1—after stage 1; T2—after stage 3 The main limitation of this study is that it is an initial pilot study. However, its strength is that the desensitization protocol is carried out with the same product and using the end point to establish the initial and follow-up dose, as of commercial juice and in three patients the direct well as the final challenge. In addition, the study allowed challenge test with peach presented no symptoms; in us to define the behavior of a group of patients during OIT two pregnant patients the final challenge test was not with peach juice, and the results obtained will enable us to performed but they were able to maintain the dose of carry out further double-blind studies. Another limitation 5 ml swallowed at home. Five patients withdrew from the of the study is that we cannot talk about the development study. The mean time taken to swallow 200 ml (T4: visit of tolerance, because there was no temporary avoidance 18 of the protocol) was 3.6 months. period preceding the challenge procedure. Future studies In most cases, the treatment allowed patients to ingest should aim to explore the possible development of foods which had previously been absent from their diet, tolerance with this desensitization protocol. Finally, the without presenting symptoms. Patients were encouraged lack of a baseline challenge, particularly in those patients to maintain regular intake of the maximum doses whose reactions occurred following dual exposure to peach reached and to avoid co-factors. and a cofactor, may be an additional limitation. In conclusion, the study demonstrates that the current protocol using a cost-effective and accessible commercial Discussion peach juice is safe and effective for desensitizing allergic Food allergy negatively affects patients’ quality of life, patients sensitized to the peach LTP Pru p 3. obliging them to avoid certain foods that are widely consumed in their environment. In order to remedy this situation, treatments such as OIT have been introduced Abbreviations ELISA: Enzyme-Linked ImmunoSorbent Assay; LTPs: lipid transfer proteins; over the last decade or so and have achieved success rates NSAIDs: non-steroidal anti-inflammatory drugs; OIT: oral immunotherapy; PBS: ranging between 40 and 90% [17–19]. phosphate buffered saline; SLIT: sublingual immunotherapy. The peach is the fruit most frequently involved in Acknowledgements food allergic reactions in the adult population in the Not applicable. Mediterranean area [2, 5]. The severity of this allergy is probably related to the high stability of its major allergen, Authors’ contributions AC-B had full access to all of the data in the study and takes responsibility Pru p 3 (which is stable to heat and digestion with pepsin) for the integrity of the data and the accuracy of the data analysis. She [20]. Sensitization to the LTP Pru p 3 has been observed contributed to the analysis and interpretation of data, drafting the case report in more than 90% of patients with peach allergy in the for important intellectual content. BN, EA and AD-P: contributed to data collection, analysis and interpretation of data, drafting the case report for Mediterranean area [21]. important intellectual content. MP and ÁC: contributed to laboratory analysis The present study demonstrates that OIT is possible and interpretation of data. All authors read and approved the final manuscript. in patients with allergy to LTPs, using a commercial Funding peach juice containing LTP as the source of the allergen. Not applicable. Previous work has demonstrated that desensitization Navarro et al. Allergy Asthma Clin Immunol (2019) 15:60 Page 6 of 6 Availability of data and materials 13. Claver A, Botey E, Navarro B, Alarcón E, Nevot S, Cisteró-Bahíma A. Early Yes introduction of baked egg (BE) in allergic patients in the first 2 years of life. Clin Transl Allergy. 2015;5(Suppl 3):P38. Ethics approval and consent to participate 14. Martorell A, Alonso E, Echeverría L, Escudero C, García-Rodríguez R, The study was approved by the local Ethics Committee and all the subjects Blasco C, Bone J, Borja-Segade J, Bracamonte T, Claver A, Corzo JL, included gave informed consent prior to participation. De la Hoz B, Del Olmo R, Dominguez O, Fuentes-Aparicio V, Guallar I, Larramona H, Martín-Muñoz F, Matheu V, Michavila A, Ojeda I, Ojeda P, Consent for publication Piquer M, Poza P, Reche M, Río PR, Rodríguez M, Ruano F, Sánchez-García Yes. S, Terrados S, Valdesoiro L, Vazquez-Ortiz M, Expert panel selected from members of the Spanish Societies of Pediatric Allergology, Asthma and Competing interests Clinical Immunology (SEICAP) and Allergology and Clinical Immunology The authors declare that they have no competing interests. (SEAIC). 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Allergy. • thorough peer review by experienced researchers in your field 2009;64:876–83. 11. Tabar AI. Oral lyophilisate and food immunotherapy: from research to • rapid publication on acceptance clinical practice. Allergol Immunopathol (Madr). 2008;36:277–9. • support for research data, including large and complex data types 12. Gomez F, Bogas G, Gonzalez M, Campo P, Salas M, Diaz-Perales A, • gold Open Access which fosters wider collaboration and increased citations Rodriguez MJ, Prieto A, Barber D, Blanca M, Torres MJ, Mayorga C. The clinical and immunological effects of sublingual immunotherapy on • maximum visibility for your research: over 100M website views per year peach and peanut allergy in patients with systemic reactions. Clin Exp Allergy. 2017;47:339–50. At BMC, research is always in progress. Learn more biomedcentral.com/submissions