t9 Olive

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• Latin name: Olea europaea
• Family: Oleaceae
• Common names: Pollen

Allergen Exposure

• Ole e 1, a 18.5-20 kDa protein, a trypsin inhibitor, a major allergen (5,7-22).
   
• Ole e 2, a 15-18 kDa protein, a profilin (5,7,23-30).
   
• Ole e 3, a 9.2 kDa protein, a 2-EF-hand calcium-binding protein (polcalcin) (5,7,27,31, 32-35).
   
• Ole e 4, a 32 kDa protein, a major allergen (7,36-38).
   
• Ole e 5, a 16 kDa protein, a superoxide dismutase. (7, 36, 37, 38, 39)
   
• Ole e 6. a 5.5-5.8 kDa protein (5,7,40-42).
   
• Ole e 7, a 9.9-10.3 kDa protein, a lipid-transfer protein, a major allergen (7,42-44).
   
• Ole e 8, a 18.8 kDa protein, a calcium-binding protein with 4 EF-hand sites and very low prevalence (7,28,32,35,40,45-46).
   
• Ole e 9, a 46.4 kDa protein, 1,3-beta-glucanase (5,7,28,47-53).
   
• Ole e 10, a 10.8 kDa protein, a glycosyl hydrolase (5,7,25,52,54).
   
• Ole e 11 (55).
   
• Ole e 36kD (56).

Not all allergens are found in every Olive tree cultivar, and most allergens isolated and characterised to date are highly polymorphic. Olive cultivars display wide differences in the expression levels of many allergens and in the number and molecular characteristics of the allergen isoforms expressed (2,57). For example, in a study examining the various IgE-binding proteins of the pollen extracts of various Olive tree cultivars, 6 predominant IgE-binding bands, some of which appeared in all the cultivars, were found. Ole e 1 appeared in only 8 of the cultivars, but not in the 9 others (58). Other authors have shown similar results, and reported that significant variations in the average reactivity of allergic patients to skin prick tests were observed, depending on the cultivar in question (59). These differences are responsible for the important differences in the allergenic potency of the extracts and have implications for the diagnosis and therapy of Olive tree pollen allergy. The prevalence of many Olive pollen allergens is dependent on geographical location. Some of the Olive allergens have been revealed to be members of known protein families, whereas no biological function has been demonstrated for Ole e 1; while Ole e 4 and Ole e 6 are proteins without known homology to other allergens (40).

Although a number of Olive tree allergens are major allergens, sensitisation is nonetheless heterogeneous. For example, in a Spanish study of Olive pollen-allergic patients, 107 (90.7%) patients had a positive skin response to Ole e 1; 88 (74.6%) reacted to Ole e 2; 57 (47.9%) reacted to both Ole e 6 and Ole e 7; and 43 (37.8%) reacted to Ole e 3. Allergenic activity determined by ELISA to Ole e 1 was found in 84%; to Ole e 2 in 61.3%; to Ole e 3 in 31.9%; to Ole e 6 in 39.4%; and to Ole e 7 in 41.2% of patients. All patients had positive skin responses to at least 1 of the allergens tested (42).

Similar results have been demonstrated in other studies. Furthermore, the IgE response to certain Olive pollen allergens is modulated by the different clinical phenotypes of allergic disease and their relationship with the level of exposure to pollen and with genetic factors (25,55,60). In a study of 146 patients with seasonal rhinitis and/or asthma and a positive prick test to Olive tree pollen, 102 (69.9%) and 79 (54.0%) patients were shown to have a significant IgE antibody response against Ole e 2 and Ole e 10, respectively. There was a significant association between Ole e 2 and Ole e 10 sensitisation and with having asthma (25,61).

In a later study, the same authors demonstrated that patients from areas of intense Olive tree pollen exposure had a complex IgE antibody response to allergens of Olive pollen, which included 3 or more allergens in 75% of cases. The majority allergens were Ole e 1, Ole e 2, Ole e 7, Ole e 9, and Ole e 10. The existence of the antigen HLA-DR2 led to a higher risk of sensitisation to Ole e 10 and a greater trend towards the development of severe asthma, which increased in the presence of anti-profilin IgE. Thirty percent of patients suffering from Olive pollen allergy also presented with allergy to vegetable foods. Anti-Ole e 7 IgE was significantly associated with fruit anaphylaxis, and anti-profilin IgE was detected in 90% of patients with oral allergy syndrome (61).

Ole e 1 is the most frequent sensitising agent of all the Olive tree allergens, affecting more than 70% of the patients with sensitisation to Olive pollen, although other antigens, such as Ole e 4 and Ole e 7, have also been shown to be major allergens (7,9,40).

The 2 Olive tree pollen calcium-binding protein allergens, Ole e 3 and Ole e 8, do not have the same structural relationships. Ole e 3, a 2-EF-hand calcium-binding protein, and Ole e 8, a calcium-binding protein with 4 EF-hand sites, have been shown to have different sensitisation profiles: 34 (17%) and 16 (8.2%) of 195 sera from Olive tree pollen-allergic patients contained IgE antibodies against
Ole e 3 and Ole e 8, respectively (35).

Sensitisation to Ole e 7 has been associated with a propensity to adverse reactions (62), and sensitivity to Ole e 10 with severe and persistent asthma (5,25).

Ole e 9, a 1,3-beta-glucanase, has been shown to be a major allergen, and has been found in the sera of 65% of patients with Olive pollinosis (47). Ole a 9 and Ole e 10 may play a role in pollen-latex-fruit syndrome (61).

A 36 kDa Olive pollen allergen has been isolated, but not characterised, and results in the sensitisation of 83% of Olive tree pollen-allergic patients. Extracts from Olive pollens collected in California demonstrated a much higher amount of the 36 kDa protein (approximately 16-fold higher) than did those from pollens of Spanish origin. The presence of similar allergens was detected in the closely related species Syringa, Fraxinus, and Ligustrum (56).

Potential cross-reactivity

A high degree of cross-reactivity has been demonstrated among Olive tree (Olea europaea), Ash (Fraxinus exselsior), Privet (Ligustrum vulgare) and Phillyrea angustifolia (a bush usually confined to certain areas of the Mediterranean), all members of the Oleaceae family, although there is no total shared identity among these 4 pollen species (63-64).

The Ole e 1-like family of proteins, which may evince cross-reactivity among members, comprises allergenic members from Oleaceae: Fra e 1 from European ash tree; Lig v 1 from Privet tree; Syr v 1 from Lilac tree; Pla l 1 from English plantain (Plantago lanceolata); Che a 1 from Goosefoot (Chenopodium album); Lol p 11 from Rye grass (Lolium perenne); and Phl p 11 from Timothy grass (Phleum pratense); as well as non-allergenic members such as BB18 from Birch tree (5,12,65-67). An 85.5 - 89.6% identity between Ole e 1 and Syr v 1 from Syringa vulgaris has been demonstrated (68).

A study comparing Olive and European ash pollen allergens, and investigating the degree of cross-reactivity in Spanish and Austrian allergic patients selectively exposed to Olive or Ash pollen, found an almost identical IgE-binding profile to both pollen allergens. A major reactivity was directed against Ole e 1 and its homologous Ash counterpart, Fra e 1. IgE inhibition experiments demonstrated extensive cross-reactivity between Olive and Ash pollen allergens. However, the study revealed that other panallergens, e.g., profilin and calcium-binding allergens, also contribute to cross-reactivity between these plants and to other unrelated plant species (16).

The relevance of Ole e 1 cross-reactivity is indicated in various situations. For example, in northern and central Europe, where there are no Olive trees, 2 common genera of the Oleaceae family, Fraxinus and Ligustrum, occur. These have a low frequency of allergic sensitisation compared to Olea, but local tests for Olive pollen sensitisation may be positive. Similarly, the importance of cross-reactivity is demonstrated by a study in Michigan, USA, where in 103 atopic subjects, cross-reactivity among Olive tree, Fraxinus, Privet and Russian Olive tree pollens was demonstrated, even though the Olive tree does not grow in that area. Nineteen subjects were skin prick-positive to this allergen, confirming cross-reactivity (3).

Cross-reactivity between extracts of Oleaceae and some species of the Poaceae family has also been shown (69-70). The major allergen of Plantago lanceolata (English plantain) pollen, Pla l 1, has been shown to have significant sequence homology with the major Olive pollen allergen Ole e 1 (71).

Ole e 2, a profilin, can be expected to result in cross-reactions with other plants containing profilin. For example, IgE antibodies directed against the Date palm pollen allergen Pho d 2 showed strong cross-reactivity with other profilins, such as those from Olive tree and grass pollens (26).

Although lipid transfer proteins are reported to be panallergens with significant cross-reactivity, Ole e 7, a lipid transfer protein, has been reported to have limited similarity with other allergenic lipid transfer proteins from vegetable sources (Peach, Apple, Cherry, Apricot, Orange, Hazelnut) and therefore no significant cross-reactivity (5).

Ole e 9, a 1,3-beta-glucanase, may result in cross-reactivity with pollens or plants containing this panallergen, e.g., Ash and Birch pollen, Tomato, Potato, Bell pepper, Banana and Latex (51).
Ole a 9 and Ole e 10 may play a role in pollen-latex-fruit syndrome (61).

As mentioned previously, a number of cross-reactive allergens may all contribute simultaneously. A study concluded that the high prevalence of Black locust tree/False acacia tree (Robinia pseudoacacia) pollen sensitisation in patients with pollinosis is likely to be due to cross-sensitisation to panallergens such as profilin, polcalcin, and 1,3-beta-glucanase from other common pollens, including Olive tree pollen (72).

A study to evaluate the associations between sensitisation to allergens of Olive tree pollen and confirmed plant-derived food allergy recruited 134 patients with allergy to Olive pollen. Only 40 reported adverse reactions to plant-derived food. Twenty-one (group A) were classified as having OAS, and 19 (group B) as having experienced anaphylaxis. In skin prick tests, sensitisation to Ole e 7 was more frequent in patients from group B. A total of 84 double-blind placebo-controlled challenges were performed, and 44% were positive. Among those who were skin prick test-positive, oral challenge confirmed the results in 68.42% for Peach, 50% for Pear, 71.42% for Melon, and 53.84% for Kiwi. In patients from group B, the following significant association with Olive tree pollen allergens were found: between positive skin prick tests for Rosaceae fruits and Ole e 3 and Ole e 7; Cucurbitaceae with Ole e 7; and Actinidiaceae with Ole e 3 (44).

Inhibition tests have found that the reactivity of the IgE antibody specific for Olive tree pollen antigen was inhibited dose-dependently by an extract of Orchard grass pollen. These findings suggest that in some patients with grass (Gramineae) pollinosis, this might be induced by Olive tree pollen (73).

A minimal-to-moderate cross-reactivity of Russian olive tree (Elaeagnus angustifolia) with Olive tree pollen was established, suggesting some cross-reactivity but not excluding co-sensitisation (74). Russian olive tree is not a member of the Oleaceae family.

An early study reported cross-reactivity among Olive, Privet, Rye grass, Couch grass and Bermuda grass pollen components but concluded that the presence of pollen-reactive IgE antibodies might not necessarily be a true reflection of the sensitising pollen species (75).

A high level of inhibition of the IgE binding of Olive pollen extract with Birch, Mugwort, Pine, and Cypress pollens was reported, suggesting that these extracts contain proteins that have common epitopes and thus can be recognised by Olive-allergic sera. The inhibition assays implied the presence of an allergen of 45 kDa (76).

In a Spanish study of Cupressus sensitisation, skin prick tests on 1532 patients with asthma and/or rhinoconjunctivitis demonstrated that of the Cupressus-sensitive patients, all also reacted positively to Olea and Fraxinus, compared to 77% and 51% in the 2 Cupressus-negative groups (77).

Cross-reactivity with Zygophyllum fabago, an herbaceous plant found widely in the Mediterranean area, has been described (78).

Clinical Experience

IgE-mediated reactions
Olive pollens can induce asthma, allergic rhinitis and allergic conjunctivitis in sensitised individuals (67,79-89).

The frequency of sensitisation to Olive tree pollen varies in the Mediterranean region from 12% in Sicily to 37% in Greece. (1, 90) In Greece, more than 37% of atopic individuals are sensitised to Oleaceae (91). Fifteen percent of atopic patients in southern France were found to be skin prick-positive to Oleaceae (92). In Italy, atopic sensitisation varied from 12.2% in Sicily to 30% in Apulia (93-97). In Naples, out of 4,142 patients examined consecutively over a 2-year period, 13.49% of adults and 8.53% of the children of all skin prick-positive patients were positive to Olea pollen allergens on skin prick testing (98). Less than 1.4% of children and 2.3% of adults were found to be monosensitised to Olive pollen (98). In a study of 507 asthmatic atopic children in the Chieti-Pescara area of Italy, skin prick tests found that 21% were sensitised to Olive tree pollen (99).

Sensitisation to Olive pollen has been reported in Israel (100-102). Positive skin reactions to Olive pollen among atopic patients of the Jewish population were shown to be high in number where Olive trees are abundant (66%), and fewer (29%) where the trees are scarce (102-103). In Spain, a study demonstrated that the frequency of sensitisation could vary greatly within the same country (104-105). Daily pollen measurements of the atmosphere showed pollen from the Olive tree to be among the most abundant pollen grains (106). Among 210 patients in the Plasencia area of Cáceres, Spain, who had a diagnosis of pollinosis, 71.9% were sensitised to Olive pollen, the second-most-prominent allergen after Cocksfoot grass (Dactylis glomerata) (80.4%) (107).

Sensitisation to Olive tree pollen has also been reported in Croatia (108), and in Cova da Beira, a central region of Portugal, where 371 paediatric patients were skin prick-tested and sensitisation to Olive tree pollen was found in 27.5% (109). Olive tree pollen has also been shown to result in sensitisation in Japan, where 16.3% of pollinosis patients were positive to this allergen (110). Skin prick tests for sensitisation to Olive tree pollen in the southern part of Switzerland (Canton Ticino) showed a high sensitisation rate of 54% (111).
The majority of studies demonstrate a higher prevalence of rhinoconjunctival symptoms than of asthma (1). Patients are more likely to be polysensitised than monosensitised to Olive tree pollen. Monosensitised individuals, children and adults, may have symptoms throughout the year without an apparent increase during the Olive pollination season (85,112).

In a Turkish study of 127 patients with respiratory allergic disease, 19 were found to be monosensitised to Olive pollen and 108 polysensitised. Of the monosensitised patients, 13 had allergic rhinitis only, while 6 had asthma as well. Of the polysensitised group, allergic rhinitis alone was present in 84, and was accompanied by asthma in 24 patients. Eleven patients with Olive tree sensitisation (57.9%) and 86 patients with polysensitisation (79.6%) had rhinitis symptoms throughout the year, irrespective of the Olive tree pollination season. Similarly, 3 of the monosensitised and 10 of the polysensitised patients with asthma had asthmatic symptoms during the pollination season and also after it (113).

Furthermore, studies in the south of Spain have demonstrated that patients exposed to extremely high Olive pollen levels display a different severity of allergy than in those exposed to normal levels, which makes it necessary to follow different treatment approaches (114).

Although Olive tree pollen allergy is broadly described in population studies, individuals working in Olive tree orchards and in laboratories are also prone. Occupational allergy was described in a researcher due to Ole e 9, an allergenic 1,3-beta-glucanase from Olive pollen. The 30-year-old researcher, involved in the study of Ole e 9-allergen and derivative recombinant products, developed nasoconjunctival pruritus, sneezing proxysms, rhinnorrhoea, conjunctival redness and palatal itching while handling fractions enriched with 35-55 kDa protein components of Olive pollen extract. He was asymptomatic during the Olive pollination season in Madrid. Skin prick tests were positive for Olive pollen and negative for other allergens tested. A single IgE-reactive band of 45 kDa was detected in the patient’s serum, and immunoblotting was positive for purified Ole e 9-allergen. The authors point out that Ole e 9 is a major allergen in areas such as Jaen, Spain, whereas patients living in Madrid, which has lower pollen counts, are notably less sensitised to Ole 9, and they are always co-sensitised to Ole e 1 (48).

Other reactions
White mustard (Sinapis alba) is an entomophilic species of the Brassicaceae family. In a study of 12 Olive orchard workers with a history of rhinitis and/or bronchial asthma that occurred during weed management and/or the harvest, from January to March, all were sensitised to S. alba pollen extract and were positive on nasal challenge testing. The study concludes that S. alba pollen is a new occupational allergen for Olive farmers (115).

Allergic reactions have been reported to ingestion of or contact with the fruit of the Olive tree (116).

Compiled by Dr Harris Steinman, harris@zingsolutions.com.

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• References