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Bringheli, I.; Brindisi, G.; Morelli, R.; Marchetti, L.; Cela, L.; Gravina, A.; Pastore, F.; Semeraro, A.; Cinicola, B.; Capponi, M.; et al. Kiwifruit’s Allergy in Children. Encyclopedia. Available online: https://encyclopedia.pub/entry/47044 (accessed on 22 June 2024).
Bringheli I, Brindisi G, Morelli R, Marchetti L, Cela L, Gravina A, et al. Kiwifruit’s Allergy in Children. Encyclopedia. Available at: https://encyclopedia.pub/entry/47044. Accessed June 22, 2024.
Bringheli, Ivana, Giulia Brindisi, Rebecca Morelli, Lavinia Marchetti, Ludovica Cela, Alessandro Gravina, Francesca Pastore, Antonio Semeraro, Bianca Cinicola, Martina Capponi, et al. "Kiwifruit’s Allergy in Children" Encyclopedia, https://encyclopedia.pub/entry/47044 (accessed June 22, 2024).
Bringheli, I., Brindisi, G., Morelli, R., Marchetti, L., Cela, L., Gravina, A., Pastore, F., Semeraro, A., Cinicola, B., Capponi, M., Gori, A., Pignataro, E., Piccioni, M.G., Zicari, A.M., & Anania, C. (2023, July 20). Kiwifruit’s Allergy in Children. In Encyclopedia. https://encyclopedia.pub/entry/47044
Bringheli, Ivana, et al. "Kiwifruit’s Allergy in Children." Encyclopedia. Web. 20 July, 2023.
Kiwifruit’s Allergy in Children
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Kiwifruit allergy is an emerging pathological condition in both general and pediatric populations with a wide range of symptoms linked to variable molecular patterns, justifying systemic and cross-reactions with other allergens (i.e., latex, pollen, and fruit). Skin prick test (SPT), specific serum IgE (Act d 1, Act d 2, Act d 5, Act d 8, and Act d 10) directed against five out of thirteen molecular allergens described in the literature, and oral test challenge with kiwifruit are available for defining diagnosis. 

kiwifruit children allergy cross-reactivity

1. Epidemiology

Acute allergy to kiwifruit was first described relatively late in 1981, by Fine [1], and nowadays it has become a major elicitor of plant food allergies. Nevertheless, the global statistics regarding the distribution of kiwifruit allergy are limited. Most research works have been conducted on the European population, although data regarding children are still lacking. In France, Rance et al., among 182 children (from 2 to 14 years of age) with a consistent history of food allergy, found that 9% were sensitized to kiwifruit [2]. The literature reports that kiwifruit allergies are often cross-reactive with others such as pollen, rye, hazelnut, chestnut, banana, and avocado. The large amount of birch trees located in Europe may elicit allergies through the cross-reactivity between birch pollen and the homologous structures found in kiwifruit protein; this may explain the larger amount of research works conducted mainly on adult European patients [3][4]. In their study, Le et al. analyzed kiwifruit allergen sensitization patterns and clinical manifestations across Europe (12 countries) in consideration of four different climatic conditions, revealing marked differences. Patients from Iceland (the only representative of northern Europe) mainly experienced severe symptoms (respiratory and cardiovascular), while most patients from central/western and southern Europe predominantly showed oral allergic syndrome (SOA). Furthermore, kiwifruit allergy associated with birch pollen allergy was most depicted in central/western Europe, while in southern Europe, the association was the highest with grass pollen allergens. Mono-allergy to kiwifruit was most frequently found in Iceland and southern Europe.

2. Molecular Allergens

Until now, thirteen allergens have been identified in kiwifruit; however, not all are accessible via in vitro diagnosis in clinical practice [5]. By far, Actinidin, also named Act d 1, represents the major allergen, since it stands for about 50% of the total soluble protein content [6]. It is frequently found in mono-sensitized patients not allergic to pollen, and is associated with the most severe symptoms. Its effect on intestinal epithelial cells is being studied. It is known that Act d 1 acts as a cysteine protease and causes a breach in the epithelial barrier, thus playing an important role in the sensitization process to kiwifruit [7]. Act d 2 is a thaumatin-like protein, and a similarity between Act d 2 and Alt a 1 has been observed both in vivo and in vitro [8]. Alt a 1 is the major allergen of Alternaria, a mold also known for the risk of fruit contamination. In fact, by penetrating the pulp, the protein Alt a 1 can establish electrostatic interactions (hydrophilic, hydrophobic, or both) with Act d 2. These interactions may cause interference with the detention capacity of dedicated diagnostic tests to detect specific IgE directed toward the native Act d 2 molecule. This has made its sensitizing prevalence unclear, given that mono-sensitization to Act d 2 is extremely rare. The clinical relevance of this association was confirmed by the high frequency of co-sensitizations observed between Act d 2 and Alt a 1 via a multimolecular test of ISAC microarrays (immuno solid-phase allergen chip): up to 85% of patients sensitized to Act d 2 were also sensitized to Alt at 1. In contrast, only 39% of patients sensitized to Alt a 1 were co-sensitized to Act d 2. Similarly, Alt a 1 could be associated with thaumatin-like PR5 proteins found in other fruits, such as cherry (Pru av 2), apple (Mal d 2), and banana (Mus a 4) [9]. Act d 3 is a 45 kDa glycoallergen, called chitinase, possibly implicated in latex fruit syndrome [10]. Act d 4 has a role in the inhibition of cysteine proteinases [11], but its clinical relevance is still unclear. Act d 5, also called Kiwellin, is a cystein-rich protein, and studies in vivo and in vitro show that a proteolytic process could split it into two additional proteins (KiTH and kissper) thanks to kiwifruit actinidin [12]. Act d 6 is a pectin methyl esterase inhibitor that possibly takes part in the regulation of the ripening of the fruit. Act d 7 is a pectin methylesterase allergen that only a small number of allergic patients are affected by [13]. Act d 8, in its composition, is very similar to Bet v 1, birch pollen’s major allergen, and it is in fact considered a pathogenesis-related protein class 10 (PR-10); this partially explains the cross-reaction, which will be discussed later on [14]. Act d 9 is a profilin which acts as a panallergen, and it can be intercepted in patients allergic to grass as well. Act d 10 is a nonspecific lipid transfer protein (LTP) and it is considered to be a minor allergen, like Act d 9 and Act d 11 [13]. Act d 11, since it is a major latex protein/ripening-related protein, usually cross-reacts with proteins of the PR-10 family [15]. Recent studies have found two new proteins in the composition of kiwifruit’s seeds: Act d 12 and Act d 13, a major and a minor allergen which share common epitopes from peanut and tree nuts, respectively, suggesting cross-reactivity with them [16][17].

3. Pathophysiology

Gut-associated lymphoid tissue is composed of innate immunity cell populations which normally react to dietary proteins with the induction of oral tolerance, which is an active inhibition of immune responses toward ingested food [18].
The pathophysiology of cross-reactions, instead, could be explained by molecular mimicry. Different allergens may share a similar stereometric conformation, which might as well trigger the mast cells by binding the IgE at the surface. Therefore, clinically significant reactions, which account for mild, moderate, or severe responses, either follow direct sensitization to the specific allergen or cross-reactions with other allergens of similar structures. The severity of symptoms is, in part, dependent upon the route of sensitization with the highest risk of severe anaphylactic reactions in those patients primarily sensitized to the allergen [18].

4. Clinical Manifestations

As with every food-related allergy, clinical manifestations vary from mild–moderate to severe reactions. The reports concerning the pediatric population are limited. Most of the information gathered in the literature has been primarily found in studies designed to explore kiwifruit cross-reactivity with other allergens in adults. Usually, the onset of symptoms occurs 2 h after kiwi exposure (ingestion or direct contact), since an IgE-mediated pattern is involved. A complete resolution of the reaction occurs within several hours. The large spectrum of clinical manifestations includes cutaneous, gastrointestinal, respiratory, cardiovascular, and neurological signs and symptoms in an isolated or concomitant manner with the same or different timing. Mild–moderate reactions might be distinguished by itching and tingling of the lips, oral mucosa, and/or itching and tingling of the tongue (oral allergy syndrome). Instead, severe reactions include urticaria or angioedema, contact urticaria, laryngeal swelling, immediate vomiting, rhinitis, cough, wheezing, bronchospasm, hypotension, loss of consciousness, and even food-dependent exercise-induced anaphylaxis [19]. As previously noted, children are more likely to develop systemic reactions involving more organs at once. For instance, Shimizu and Morikawa reported a case of a 12-year-old boy with atopic dermatitis and allergic rhinitis who developed anaphylaxis after 15 min from the second ingestion of kiwi in his life. The kiwi-specific IgE level and the skin prick test were positive [20]. Also, Rance et al. reported a case of a 3-year-old boy and an 8-year-old girl rapidly developing hypotensive shock after handling kiwifruit [21]. A recent Italian study including 25 patients confirmed that the most frequent symptoms are angioedema and urticaria followed by AOS, gastrointestinal symptoms, rhinoconjunctivitis, cough, and dyspnea, while anaphylaxis was described in six patients. All of the patients tested positive for the allergen extracted via the skin tests and for specific IgE [22]. The severity of reactions is useful for suspecting the precise molecular pattern of sensitization involved. Being able to distinguish, on a molecular basis, between primary or cross-reactive reactions nowadays represents a great resource for proper management.

5. Diagnosis

Patient clinical history and examination are the first steps toward a diagnosis of kiwifruit allergy [23]. Other clinical diagnostic tools include skin prick test (SPT), enzyme-linked immunosorbent assay (ELISA), component-resolved diagnosis (CRD), and double-blind placebo-controlled food challenge (DBPCFC) [24]. DBPCFC is considered to be the gold standard test to detect a food allergy because it ensures an objective assessment of outcomes without operator-specific preconceptions or biases [25]. However, it is logistically demanding, and anaphylactic reactions may occur. Therefore, if the anamnesis is suggestive, an SPT is performed as a more accessible diagnostic tool to identify IgE-specific sensitization (95%) [26]. D’Amelio et al. [27] found low sensitivity when an SPT was applied using commercial kiwifruit extracts (52.8–66.7%), while a prick by prick test with fresh kiwifruit yielded the highest sensitivity (81.8%); hence, it has been shown that it preserves kiwi allergenic proteins, ensuring good diagnostic capacity [12]. ELISA and immunoCAP (a commercial ELISA) are two similar blood test methods based on the detection of specific serum IgE. Reports to date are contradictory about the role of measuring specific IgE to confirm kiwifruit allergy. Lucas et al. [19] found the test to have good specificity (83%) and poor sensitivity (60%), with the latter being most probably related to the lability of allergens, as it had already been identified in the skin test solution. Furthermore, the study revealed that the level of specific IgE was not correlated with the reported severity of symptoms or age. It is noteworthy that serum IgE toward kiwifruit extract (ELISA/ImmunoCAP) corresponds to the detection rate of CRD in recognizing Act d 1, the major kiwifruit allergen [26]. Bublin M. et al., by applying CRD, managed to classify adult patients in different reactor groups: [11] actinidin (Act d 1) may serve as a marker for isolated kiwifruit allergy, while Act d 8 and Act d 9 might be indicative of typical cross-reactivity patterns. As previously described, the clinical association of pollinosis with an allergy to fresh fruit, including kiwi, is well recognized indeed [28]. Many allergens in kiwifruit are readily digested by simulated gastric fluid; this may explain why most allergic reactions are restricted to the oral cavity (OAS) in adults with a pollen allergy. The aforementioned study on a cohort of 25 Italian children also specified that the allergens (Act d 8, Bet v1) linked to pollen–fruit syndrome could also be associated with sensitization to Act d 1, the major stable antigen, thus explaining the risk of severe systemic reactions [22]. Moreover, the potential gastrointestinal route of sensitization could expose different allergens or combinations of allergens from kiwifruit that may elicit more severe clinical manifestations in children [29]. Therefore, the introduction of CRD represents a useful tool which needs to be further investigated in the diagnostic process toward a definition of kiwifruit allergies.

References

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  2. Rancé, F.; Grandmottet, X.; Grandjean, H. Prevalence and main characteristics of schoolchildren diagnosed with food allergies in France. Clin. Exp. Allergy 2005, 35, 167–172.
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  8. Saenz-De-Santamaria, M.; Postigo, I.; Gutierrez-Rodriguez, A.; Cardona, G.; Guisantes, J.A.; Asturias, J.; Martinez, J. The major allergen of Alternaria alternata (Alt a 1) is expressed in other members of the Pleosporaceae family. Mycoses 2006, 49, 91–95.
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  12. Tamburrini, M.; Cerasuolo, I.; Carratore, V.; Stanziola, A.A.; Zofra, S.; Romano, L.; Camardella, L.; Ciardiello, M.A. Kiwellin, a novel protein from kiwi fruit. Purification, biochemical characterization and identification as an allergen. Protein J. 2005, 24, 423–429.
  13. Bublin, M.; Dennstedt, S.; Buchegger, M.; Ciardiello, M.A.; Bernardi, M.L.; Tuppo, L.; Harwanegg, C.; Hafner, C.; Ebner, C.; Ballmer-Weber, B.K.; et al. The performance of a component-based allergen microarray for the diagnosis of kiwifruit allergy. Clin. Exp. Allergy. 2011, 41, 129–136.
  14. Oberhuber, C.; Bulley, S.M.; Ballmer-Weber, B.K.; Bublin, M.; Gaier, S.; DeWitt, M.; Briza, P.; Hofstetter, G.; Lidholm, J.; Vieths, S.; et al. Characterization of Bet v 1-related allergens from kiwifruit relevant for patients with combined kiwifruit and birch pollen allergy. Mol. Nutr. Food Res. 2008, 52 (Suppl. S2), S230–S240.
  15. D’Avino, R.; Bernardi, M.L.; Wallner, M.; Palazzo, P.; Camardella, L.; Tuppo, L.; Alessandri, C.; Breiteneder, H.; Ferreira, F.; Ciardiello, M.A.; et al. Kiwifruit Act d 11 is the first member of the ripening-related protein family identified as an allergen. Allergy 2011, 66, 870–877.
  16. Sirvent, S.; Cantó, B.; Gómez, F.; Blanca, N.; Cuesta-Herranz, J.; Canto, G.; Blanca, M.; Rodríguez, R.; Villalba, M.; Palomares, O. Detailed characterization of Act d 12 and Act d 13 from kiwi seeds: Implication in IgE cross-reactivity with peanut and tree nuts. Allergy 2014, 69, 1481–1488.
  17. Asaumi, T.; Yanagida, N.; Sato, S.; Takahashi, K.; Ebisawa, M. Negative Act d 8 indicates systemic kiwifruit allergy among kiwifruit-sensitized children. Pediatr. Allergy Immunol. 2017, 28, 291–294.
  18. Van Wijk, F.; Knippels, L. Initiating mechanisms of food allergy: Oral tolerance versus allergic sensitization. Biomed. Pharmacother. 2007, 61, 8–20.
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  23. Muraro, A.; Werfel, T.; Hoffmann-Sommergruber, K.; Roberts, G.; Beyer, K.; Bindslev-Jensen, C.; Cardona, V.; Dubois, A.; Dutoit, G.; Eigenmann, P.; et al. EAACI food allergy and anaphylaxis guidelines: Diagnosis and management of food allergy. Allergy 2014, 69, 1008–1025.
  24. Jeon, Y.H.; Ahn, K.; Kim, J.; Shin, M.; Hong, S.-J.; Lee, S.-Y.; Pyun, B.Y.; Min, T.K.; Jung, M.; Lee, J.; et al. Clinical Characteristics of Atopic Dermatitis in Korean School-Aged Children and Adolescents According to Onset Age and Severity. J. Korean Med. Sci. 2022, 37, e30.
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  29. Moreno Álvarez, A.; Sexto, L.V.; Bardina, L.; Grishina, G.; Sampson, H.A. Kiwifruit Allergy in Children: Characterization of Main Allergens and Patterns of Recognition. Children 2015, 2, 424–438.
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