IgE to cyclophilins in pollen-allergic children: Epidemiologic, clinical, and diagnostic relevance of a neglected panallergen

https://www.jacionline.org/article/S0091-6749(24)00235-5/fulltext

The Journal of Allergy and Clinical Immunology, Rhinitis, sinusitis, and ocular allergy| Volume 153, ISSUE 6, P1586-1596.e2, June 2024. Published: March 18, 2024. DOI: https://doi.org/10.1016/j.jaci.2024.01.030

Paolo Maria Matricardi, MD, Ekaterina Potapova, MD, Valentina Panetta, PhD, Jonas Lidholm, PhD, Lars Mattsson, PhD, Enrico Scala, MD, Roberto Bernardini, MD, Carlo Caffarelli, MD, Antonella Casani, MD, Rosa Cervone, MD, Loredana Chini, MD, Pasquale Comberiati, MD, Giovanna De Castro, MD, Michele Miraglia del Giudice, MD, Iride Dello Iacono, MD, Andrea Di Rienzo Businco, MD, Marcella Gallucci, MD, Arianna Giannetti, MD, Viviana Moschese, MD, Elena Varin, MD, Annamaria Bianchi, MD, Mauro Calvani, MD, Tullio Frediani, MD, Francesco Macrì, MD, Nunzia Maiello, MD, Francesco Paravati, MD, Umberto Pelosi, MD, Diego Peroni, MD, Giuseppe Pingitore, MD, Mariangela Tosca, MD, Anna Maria Zicari, MD, Giampaolo Ricci, MD, Riccardo Asero, MD, Salvatore Tripodi, MD for theItalian Pediatric Allergy Network

Background

Cyclophilins are ubiquitous panallergens whose epidemiologic, diagnostic, and clinical relevance is largely unknown and whose sensitization is rarely examined in routine allergy practice.

Objective

We investigated the epidemiologic, diagnostic, and clinical relevance of cyclophilins in seasonal allergic rhinitis and its comorbidities.

Methods

We examined a random sample of 253 (25%) of 1263 Italian children with seasonal allergic rhinitis from the Panallergens in Pediatrics (PAN-PED) cohort with characterized disease phenotypes. Nested studies of sensitization prevalence, correlation, and allergen extract inhibition were performed in patients sensitized to birch pollen extract but lacking IgE to Bet v 1/2/4 (74/1263) or with highest serum level of IgE to Bet v 1 (26/1263); and in patients with sensitization to various extracts (ragweed, mugwort, pellitory, Plantago, and plane tree), but not to their respective major allergenic molecule, profilins, and polcalcins. IgE to cyclophilin was detected with recombinant Bet v 7, and extract inhibition tests were performed with the same rBet v 7.

Results

IgE to rBet v 7 was detected in 43 (17%) of 253 patients. It was associated with asthma (P < .028) and oral allergy syndrome (P < .017) in univariate but not multivariate analysis adjusted for IgE to profilins (Phl p 12), PR-10s (Bet v 1), and lipid transfer proteins (Pru p 3). IgE to rBet v 7 was also highly prevalent (47/74, 63%) among patients with unexplained sensitization to birch pollen extract. In patients with unexplained sensitization to ragweed, mugwort, pellitory, Plantago and plane tree pollen, the levels of IgE to those extracts correlated with the levels of IgE to rBet v 7, and they were also significantly inhibited by rBet v 7 (inhibition range 45%-74%).

Conclusions

IgE sensitization to cyclophilin is frequent in pollen-allergic patients living in temperate areas and can produce “false” positive outcomes in skin prick and IgE tests to pollen extracts. Molecular diagnostic guidelines should include this panallergen family.

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