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Double-Blind, Randomized, Placebo-Controlled Trial of Allergen-Specific Immunotherapy with the Major Allergen Alt a 1

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Double-Blind, Randomized, Placebo-Controlled Trial of Allergen-Specific Immunotherapy with the Major Allergen Alt a 1 Double-blind, randomized, placebo-controlled trial of allergen-specific immunotherapy with the major allergen Alt a 1 Ana Isabel Tabar, MD, PhD,a Luis Prieto, MD, PhD,b Pilar Alba, MD,c Antonio Nieto, MD, PhD,d Mercedes Rodrıguez, MD,e Miguel Torrecillas, MD,f Beatriz Huertas, MD,g Elisa Gomez, MD, PhD,h Francisco Javier Fernandez, MD, PhD,i Miguel Blanca, MD, PhD,j David Rodrıguez, PhD,k and Ricardo Palacios, PhDk Pamplona, Valencia, Madrid, Albacete, Ciudad Real, Alicante, and Malaga, Spain GRAPHICAL ABSTRACT Background: There have been few studies conducted on the efficacy a 1. Recorded adverse reactions were graded according to and safety of specific immunotherapy with allergen extracts of fungi World Allergy Organization criteria. compared with other allergen extracts, and there are no data on the Results: There were significant reductions in the combined major allergen Alt a 1 of the fungus Alternaria alternata. symptom and medication score for the 0.37-mg dose of Alt a 1 Objectives: We sought to evaluate the efficacy and safety of compared with placebo at 12 months of treatment. Reduced subcutaneous immunotherapy with 2 different doses of Alt a 1 cutaneous reactivity and IgE levels, together with increased A in patients with rhinoconjunctivitis caused by sensitization to IgG4 levels, were demonstrated for the 2 active groups versus alternata. the placebo group. A similar safety profile was found for both Method: We performed a multicenter, randomized, double- active groups compared with the placebo group. No serious blind, placebo-controlled trial with Alt a 1 administered adverse drug reactions were reported. subcutaneously in patients with allergic rhinoconjunctivitis with Conclusion: Immunotherapy with Alt a 1 was efficacious and or without controlled asthma aged 12 to 65 years. Three groups safe, reducing the symptoms and medication consumption were included: the placebo group and active groups receiving associated with rhinoconjunctivitis after only 1 year of 0.2 or 0.37 mg of Alt a 1 per dose. The main end point was the treatment. The clinical benefits were associated with reduced combined symptom and medication score. Secondary end points skin reactivity and specific IgE levels and increased IgG4 levels. were cutaneous reactivity and serum IgE and IgG4 levels to Alt (J Allergy Clin Immunol 2019;144:216-23.) From aComplejo Hospitalario de Navarra, Pamplona; bHospital Universitario Dr. Peset, Received for publication May 18, 2018; revised January 22, 2019; accepted for publica- Valencia; cHospital de Manises, Valencia; dHospital Universitario La Fe, Valencia; tion February 8, 2019. eHospital Universitario Prıncipe de Asturias, Alcala de Henares, Madrid; fHospital Available online March 14, 2019. Universitario Nuestra Senora~ del Perpetuo Socorro, Albacete; gHospital del Sureste, Corresponding author: David Rodrıguez, PhD, Diater Laboratorios S.A., Avenida Arganda del Rey, Madrid; hHospital Universitario de Ciudad Real; iHospital General, Gregorio Peces Barba no2, Leganes, Madrid, 28918 Spain. E-mail: d.rodriguez@ Universitario de Alicante; jHospital Regional Universitario Carlos Haya, Malaga; and diater.com. kDiater Laboratorios S.A., Leganes, Madrid. The CrossMark symbol notifies online readers when updates have been made to the Supported by Laboratorios Diater S.A., Leganes, Madrid, Spain. article such as errata or minor corrections Disclosure of potential conflict of interest: A. I. Tabar reports and declares that she is the 0091-6749 Ó coordinating investigator of the clinical trial. D. Rodrıguez and R. Palacios report and 2019 The Authors. Published by Elsevier Inc. on behalf of the American Academy of declare that they are employees of the company sponsoring the clinical trial, Diater Allergy, Asthma & Immunology. This is an open access article under the CC BY-NC- Laboratorios. The rest of the authors declare that they have no relevant conflicts of ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). interest. https://doi.org/10.1016/j.jaci.2019.02.029 216 J ALLERGY CLIN IMMUNOL TABAR ET AL 217 VOLUME 144, NUMBER 1 Key words: Allergen immunotherapy, clinical trial, Alt a 1, molecular immunotherapy, rhinoconjunctivitis, efficacy, safety, Abbreviations used fungal allergy, subcutaneous immunotherapy, purified allergen, ADR: Adverse drug reaction adults, children AE: Adverse event CRF: Case report form Alternaria species represent probably the most important CSMS: Combined symptom and medication score saprophytic genus from the fungal allergy point of view.1 ITT: Intention to treat Alternaria alternata is the most abundant and best studied PP: Per-protocol WAO: World Allergy Organization species, given its importance as an aeroallergen with a worldwide distribution and a high rate of involvement in patients with allergic diseases, such as rhinitis and asthma.2 A alternata predominates in outdoor environments, and its spores are principally involved in sensitization,3 although its categorization or without mild or moderate asthma were recruited.17 The patients’ and importance as an indoor allergen have also been established.4 sensitization was demonstrated, and skin test follow-up was performed Alt a 1 is the predominant allergen of the 17 reactive IgE proteins throughout the trial by using skin prick tests (wheal diameter >_3 mm) with 5 whole extract of A alternata (2HEPD) and the major allergen, purified natural identified in A alternata, 12 of which are described in m the International Union of Immunological Societies Alt a 1, at a concentration of 10 g/mL (Diater, Madrid, Spain). Levels of 6 specific IgE to Alt a 1 were determined by using a commercially available (www.allergen.org). It is mainly present in the spore wall and system (Thermo Fisher Scientific, Waltham, Mass), with a cutoff value of responds molecularly to a 30-kDa dimer specific to the Fungi 0.7 kU/L or greater. Patients polysensitized to epithelia and mites were not kingdom, with a b-barrel structure and an unknown biological func- selected for this study nor were those with uncontrolled asthma and those 7 tion. In reducing conditions it can be separated into subunits of 16.4 who had received fungal immunotherapy in the 3 years before initiation of and 15.3 kDa, respectively. Sensitization to Alt a 1 is identified in the trial. more than 90% of patients with allergy to A alternata.2,5 We recruited 113 patients, 111 of whom received at least 1 administration The availability of Alt a 1 isolated in its natural form for use in (intention to treat [ITT]), who were assigned as follows: 29 to placebo, 37 to in vivo diagnoses and immunotherapy provides an alternative to low-dose Alt a 1 (0.2 mg of Alt a 1/dose), and 45 to high-dose Alt a 1 (0.37 mgof the variability of whole allergenic extracts from molds.8,9 Alt a Alt a 1/dose, Fig 2): 66 were male (59.5%) and 45 were female (40.5%) subjects, 1 is not present only in A alternata but is an orthologous allergen and 63 (56.8%) were aged 18 years or more and 48 (43.2%) were aged 17 years or less. The mean age was 21 years (SD, 8 years; range, 12–44 years). present in other species of the order Pleosporales, such as Stemphylium botryosum and Ulocladium botrytis. This would make it possible to apply the diagnosis and treatment with Alt a 10-12 Immunotherapy with Alt a 1 1 to patients sensitized to these fungi as well. The major allergen Alt a 1 isoform 1.0101 (UniProt P79085) was purified After a first clinical trial, classified as phase IV by the Agencia from an extract of A alternata by using ion exchange and size exclusion Espanola~ de Medicamentos y Productos Sanitarios, which chromatography, with a purity of greater than 95%.13 demonstrated the safety of treatment with Alt a 1 in patients Alt a 1 was stabilized by means of lyophilization in single-dose vials with with symptoms of rhinitis and asthma caused by sensitization to A mannitol as a cryoprotectant at concentrations of 0.025 mg per vial and alternata,13 the aim of this trial was to evaluate the efficacy and 0.046 mg per vial for the induction dose and 0.25 mg per vial and 0.46 mg per safety of a higher dose of Alt a 1 and compare it with the vial for the maintenance dose. Physiologic saline was used as the diluent, with previously tested dose. aluminum hydroxide (0.83 mg per vial) as an adjuvant. The maximum volume of subcutaneous administration was 0.8 mL. METHODS Trial end points Trial design The main study end point was the combined symptom and medication score (CSMS). Nasal symptoms recorded were nasal congestion, pruritus, mucus A multicenter, randomized, double-blind, parallel-group, placebo-controlled production, and sneezing. A score based on symptom severity was used: 0, clinical trial of differing concentrations of Alt a 1 was designed. Randomization no symptoms; 1, mild symptoms; 2, moderate symptoms; and 3, severe was carried out by the sponsor in blocks of 6 for each participating hospital. The symptoms. Ocular symptoms recorded were hyperemia, pruritus, tearing, and treatments were assigned on a 1:1:1 basis so that each block of 6 contained 2 exudate; an identical severity score was used. The score of each symptom was high-dose treatments, 2 low-dose treatments, and 2 placebos. The trial was added up, resulting in a score ranging from 0 to 24. The result was then divided authorized by the Clinical Research Ethics Committee, Hospital Complex of by the number of symptoms evaluated, resulting in a final symptom score Navarra, Spain, and the Spanish Agency of Medicines and Medical Devices ranging from 0 to 3. All patients had access to identical rescue medication (EudraCT 2010-024440-15) and included 113 patients from 17 Spanish when necessary. Medication use was graded as follows: 0, no rescue hospitals.
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