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Anaphylaxis resulting from selective sensitization to Americana grapes
J ALLERGY CLIN IMMUNOL VOLUME 104, NUMBER 5
Bircher, Bigliardi, and Yilmaz 1111
Anaphylaxis resulting from selective sensitization to Americana grapes Andreas J. Bircher, MD, Paul Bigliardi, MD, and Bilgehan Yilmaz, MD Basel, Switzerland Key words: Anaphylaxis, grapes, sensitization, prick-to-prick test
Grapes (Vitis vinifera L.) are grown in temperate and subtropical climate zones on all continents for consumption and the production of wine. Although the pollenassociated oral allergy syndrome to fresh fruits is common, allergic reactions to grapes have been rarely reported. In some earlier articles grapes are mentioned among other foods as allergens in patients allergic to pollen1,2; however, tests have not been performed. Only recently have patients with allergic reactions to grapes been described in detail.3-5 We report a patient without previous atopic diseases who had a selective sensitization to one grape species, resulting in repeated anaphylactic reactions.
CASE REPORT A 44-year-old man was referred for investigation of several anaphylactic reactions that had all occurred in autumn. Within 3 years he had had 4 episodes with palmoplantar pruritus, urticaria, dyspnea, dysphagia, gastric pain, sweating, and tachycardia, which all occurred at night. A detailed history revealed that 4 to 6 hours
From the Allergy Unit, Department of Dermatology, University Hospital, Basel, Switzerland. Received for publication Mar 5, 1999; revised July 19, 1999; accepted for publication July 20, 1999. Reprint requests: Andreas J. Bircher, MD, Allergy Unit, Department of Dermatology, University Hospital, CH-4031 Basel, Switzerland. J Allergy Clin Immunol 1999;104:1111-3. Copyright © 1999 by Mosby, Inc. 0091-6749/99 $8.00 + 0 1/54/101662
Abbreviation used CAP-RAST: Radioallergosorbent test
before every allergic reaction he had eaten large amounts of selfgrown red Americana grapes. He had no history of atopic diseases, food allergy including oral allergy syndrome, or drug hypersensitivity and he still ate large amounts of fruits and different species of other red and white grapes, and he drank grape juice and red and white wine without allergic symptoms. Skin prick tests with commercial allergens (grass, rye, birch, alder, hazel, ash, beech, plantain, sorrel and mugwort pollens, house dust mites, cat and dog danders, latex, Aspergillus fumigatus, Penicillium notatum, Alternaria alternata, Cladosporium herbarum) were positive to A fumigatus and Aspergillus mix only. Prick-toprick tests6 were performed with raisins and grape juice and with different species of fresh grapes in the following manner: a singleuse standard prick needle was inserted into the respective grape or raisin and then used on the skin of the back. The test was defined as positive with a wheal diameter of at least 3 mm indicated by a + reaction. Grapes were tested (1) as is, (2) surface cleaned with absolute ethanol, and (3) briefly (~30 sec) heated in a microwave oven. They were positive to Americana grapes only (patient’s own and commercial brand) (Table I). Ten patients with positive skin tests to respiratory allergens were tested with Americana grapes as is. Nine control subjects had negative results, and one woman who had throat itching after eating Americana grapes had a + positive reaction to Americana grapes. All tested grapes were cultured for molds. Penicillium sp was detected on several grape species including on Americana. Aspergillus sp was cultured from one brand of red raisins (Table I). Total IgE was 42 kU/L; a multispecific screening test (Phadiatop
1112 Bircher
J ALLERGY CLIN IMMUNOL NOVEMBER 1999
TABLE I. Results of skin tests and cultures with grapes and raisins Prick-to-prick tests Grapes and raisins
Histamine hydrochloride 10 mg/mL Negative control A fumigatus/mix Americana (red, patient’s own) Americana (red, commercial) Lavallé (red) Uva italia (red) Seyval (white) Chasselas (white) Moissac (white) Raisins (red) Raisins (red, health food store) Raisins (white) Grape juice (red)
As is
Ethanol cleaned
Microwave heated
++ – +/+ ++ + – – – – – – – – –
NA NA NA + + – – – – – – – – –
NA NA NA + + – – – – – – – – –
Fungal culture
NA NA NA Penicillium sp Candida sp Penicillium sp Penicillium sp Penicillium sp Alternaria sp Alternaria sp Mucor sp Aspergillus niger — —
NA, Not applicable.
or SX-1 measuring the presence of specific IgE to grass, rye, birch, mugwort pollen, cat, dog, Dermatophagoides pteronyssinus and Cladosporium) was negative (<0.35 kU/L = class 0). Specific IgE was 3.74 kU/L (class 3) to Aspergillus sp and <0.35 kU/L to P notatum and grapes (f 259). An attempt to measure IgE by the ImmunoCAP method to Americana by coupling extracts (courtesy of Pharmacia-Upjohn) failed to give positive results.
DISCUSSION Allergic reactions to grapes have been rarely reported. In a case from Germany a 43-year-old man had angioedema to plums and to white and red grapes with positive prick-to-prick tests and specific IgE to grape extracts.3 Exercise-induced anaphylaxis to grapes has been observed in a Japanese patient,4 and 2 French patients with initially oral allergy syndrome to red grapes later had anaphylaxis.5 They had positive skin tests and IgE to red grapes. Recently, 3 patients with anaphylaxis to grapes with positive skin tests and radioallergosorbent (CAP-RAST) tests to grapes have been described.7 A 28year-old woman with high total IgE (1918 ng/mL) who had recurrent anaphylaxis after eating white grapes had positive skin prick tests to commercial grape extracts and specific IgE to grapes (class 1).8 In a 4-year-old boy who had urticaria and angioedema to grapes, raisins, and a variety of other fruits and vegetables, positive skin tests and IgE to a large number of foods and respiratory allergens including grapes were observed.9 Finally, a 24-yearold man with an oral allergy syndrome to grapes and red and white wines with positive skin tests and specific IgE to grapes has been described.10 Our patient had several anaphylactic reactions up to 6 hours after the ingestion of Americana grapes, whereas other grapes were skin-test negative and were well tolerated. Selective sensitization to Aspergillus and Americana grapes was found, but the demonstration of Americana-specific IgE failed, possibly because of the method used. In the preparation of RAST tests the production of polyphenols in plant cells should be taken into account to
prevent false-negative test results, as it has been recently demonstrated.10 Also the commercial allergen skin tests and commercial CAP-RAST to grapes were negative. The delay of several hours between the ingestion and the occurrence of symptoms is unusual. It may be due to the oral uptake of the allergen and a slow absorption in combination with a relatively stable allergen. The latter is supported by the positive prick tests with heated grapes as it has been also shown in another patient.3 The negative skin tests to and the clinical tolerance of other grapes suggest a specific allergen in Americana grapes. Aspergillus as a contaminating allergen is unlikely because it was not found on cultured Americana grapes, and skin tests with ethanol-cleaned grapes were also positive. Since the patient has avoided Americana grapes, he has had no further anaphylactic reactions. Some patients with grape allergy have atopic diseases and there appears to be some cross-reactivity to other foods such as cherry,10 plum,3 banana, kiwi, and chestnut7 on the basis of clinical grounds and on RAST inhibition tests. Other patients,8 as our case, have no previous atopic diseases and are monosensitized to grapes. Grapes should be added to the increasing number of fruits that elicit oral allergic symptoms and sometimes more severe reactions such as anaphylaxis. When commercial skin test extracts are negative, fresh grapes should be tested by the prick-to-prick method. REFERENCES 1. Eriksson N. Food sensitivity reported by patients with asthma and hay fever. Allergy 1978;33:189-96. 2. Eriksson N, Formgren H, Svenonius E. Food hypersensitivity in patients with pollen allergy. Allergy 1982;37:437-43. 3. Senff H, Hausen BM, Exner M, Kalveram KJ, Goos M. Pflaumen- und Weintraubenallergie – ein Fallbericht. Pollenassoziierte Obstallergien und ihre Diagnostik. Z Hautkr 1990;66:337-40. 4. Dohi M, Suko M, Sugiyama H, Yamashita N, Tadokoro K, Juji F, et al. Food-dependent, exercise-induced anaphylaxis: a study on 11 Japanese cases. J Allergy Clin Immunol 1991;87:34-40. 5. Guinnepain M-T, Rassemont R, Laurent J. Le raisin est aussi un trophallergène. Rev Fr Allergol 1997;37:400.
J ALLERGY CLIN IMMUNOL VOLUME 104, NUMBER 5
6. Dreborg S, editor. Skin tests used in type I allergy testing [position paper]. Allergy 1989;44(10 Suppl):44-51. 7. Anton E, Jiménez I, Polo F, Picáns I, Sánchez I, Jerez J. Immediate hypersensitivity to grape: study of cross-reactivity with other fruits. Allergy 1997;52(37 Suppl):119. 8. Vaswani SK, Hamilton RG, Carey RN, Chang BW. Anaphylaxis, recur-
1113
rent urticaria and angioedema from grape hypersensitivity [abstract]. J Allergy Clin Immunol 1998;101(Suppl):S31. 9. Romano C, Ferrara A. Food allergy induced by grapes. Allergy 1998;53:93. 10. Giannoccaro F, Munno G, Riva G, Pugliese S, Paradiso M, Ferrannini A. Oral allergy syndrome to grapes. Allergy 1998;53:451-2.
Bircher, Bigliardi, and Yilmaz 1111
Anaphylaxis resulting from selective sensitization to Americana grapes Andreas J. Bircher, MD, Paul Bigliardi, MD, and Bilgehan Yilmaz, MD Basel, Switzerland Key words: Anaphylaxis, grapes, sensitization, prick-to-prick test
Grapes (Vitis vinifera L.) are grown in temperate and subtropical climate zones on all continents for consumption and the production of wine. Although the pollenassociated oral allergy syndrome to fresh fruits is common, allergic reactions to grapes have been rarely reported. In some earlier articles grapes are mentioned among other foods as allergens in patients allergic to pollen1,2; however, tests have not been performed. Only recently have patients with allergic reactions to grapes been described in detail.3-5 We report a patient without previous atopic diseases who had a selective sensitization to one grape species, resulting in repeated anaphylactic reactions.
CASE REPORT A 44-year-old man was referred for investigation of several anaphylactic reactions that had all occurred in autumn. Within 3 years he had had 4 episodes with palmoplantar pruritus, urticaria, dyspnea, dysphagia, gastric pain, sweating, and tachycardia, which all occurred at night. A detailed history revealed that 4 to 6 hours
From the Allergy Unit, Department of Dermatology, University Hospital, Basel, Switzerland. Received for publication Mar 5, 1999; revised July 19, 1999; accepted for publication July 20, 1999. Reprint requests: Andreas J. Bircher, MD, Allergy Unit, Department of Dermatology, University Hospital, CH-4031 Basel, Switzerland. J Allergy Clin Immunol 1999;104:1111-3. Copyright © 1999 by Mosby, Inc. 0091-6749/99 $8.00 + 0 1/54/101662
Abbreviation used CAP-RAST: Radioallergosorbent test
before every allergic reaction he had eaten large amounts of selfgrown red Americana grapes. He had no history of atopic diseases, food allergy including oral allergy syndrome, or drug hypersensitivity and he still ate large amounts of fruits and different species of other red and white grapes, and he drank grape juice and red and white wine without allergic symptoms. Skin prick tests with commercial allergens (grass, rye, birch, alder, hazel, ash, beech, plantain, sorrel and mugwort pollens, house dust mites, cat and dog danders, latex, Aspergillus fumigatus, Penicillium notatum, Alternaria alternata, Cladosporium herbarum) were positive to A fumigatus and Aspergillus mix only. Prick-toprick tests6 were performed with raisins and grape juice and with different species of fresh grapes in the following manner: a singleuse standard prick needle was inserted into the respective grape or raisin and then used on the skin of the back. The test was defined as positive with a wheal diameter of at least 3 mm indicated by a + reaction. Grapes were tested (1) as is, (2) surface cleaned with absolute ethanol, and (3) briefly (~30 sec) heated in a microwave oven. They were positive to Americana grapes only (patient’s own and commercial brand) (Table I). Ten patients with positive skin tests to respiratory allergens were tested with Americana grapes as is. Nine control subjects had negative results, and one woman who had throat itching after eating Americana grapes had a + positive reaction to Americana grapes. All tested grapes were cultured for molds. Penicillium sp was detected on several grape species including on Americana. Aspergillus sp was cultured from one brand of red raisins (Table I). Total IgE was 42 kU/L; a multispecific screening test (Phadiatop
1112 Bircher
J ALLERGY CLIN IMMUNOL NOVEMBER 1999
TABLE I. Results of skin tests and cultures with grapes and raisins Prick-to-prick tests Grapes and raisins
Histamine hydrochloride 10 mg/mL Negative control A fumigatus/mix Americana (red, patient’s own) Americana (red, commercial) Lavallé (red) Uva italia (red) Seyval (white) Chasselas (white) Moissac (white) Raisins (red) Raisins (red, health food store) Raisins (white) Grape juice (red)
As is
Ethanol cleaned
Microwave heated
++ – +/+ ++ + – – – – – – – – –
NA NA NA + + – – – – – – – – –
NA NA NA + + – – – – – – – – –
Fungal culture
NA NA NA Penicillium sp Candida sp Penicillium sp Penicillium sp Penicillium sp Alternaria sp Alternaria sp Mucor sp Aspergillus niger — —
NA, Not applicable.
or SX-1 measuring the presence of specific IgE to grass, rye, birch, mugwort pollen, cat, dog, Dermatophagoides pteronyssinus and Cladosporium) was negative (<0.35 kU/L = class 0). Specific IgE was 3.74 kU/L (class 3) to Aspergillus sp and <0.35 kU/L to P notatum and grapes (f 259). An attempt to measure IgE by the ImmunoCAP method to Americana by coupling extracts (courtesy of Pharmacia-Upjohn) failed to give positive results.
DISCUSSION Allergic reactions to grapes have been rarely reported. In a case from Germany a 43-year-old man had angioedema to plums and to white and red grapes with positive prick-to-prick tests and specific IgE to grape extracts.3 Exercise-induced anaphylaxis to grapes has been observed in a Japanese patient,4 and 2 French patients with initially oral allergy syndrome to red grapes later had anaphylaxis.5 They had positive skin tests and IgE to red grapes. Recently, 3 patients with anaphylaxis to grapes with positive skin tests and radioallergosorbent (CAP-RAST) tests to grapes have been described.7 A 28year-old woman with high total IgE (1918 ng/mL) who had recurrent anaphylaxis after eating white grapes had positive skin prick tests to commercial grape extracts and specific IgE to grapes (class 1).8 In a 4-year-old boy who had urticaria and angioedema to grapes, raisins, and a variety of other fruits and vegetables, positive skin tests and IgE to a large number of foods and respiratory allergens including grapes were observed.9 Finally, a 24-yearold man with an oral allergy syndrome to grapes and red and white wines with positive skin tests and specific IgE to grapes has been described.10 Our patient had several anaphylactic reactions up to 6 hours after the ingestion of Americana grapes, whereas other grapes were skin-test negative and were well tolerated. Selective sensitization to Aspergillus and Americana grapes was found, but the demonstration of Americana-specific IgE failed, possibly because of the method used. In the preparation of RAST tests the production of polyphenols in plant cells should be taken into account to
prevent false-negative test results, as it has been recently demonstrated.10 Also the commercial allergen skin tests and commercial CAP-RAST to grapes were negative. The delay of several hours between the ingestion and the occurrence of symptoms is unusual. It may be due to the oral uptake of the allergen and a slow absorption in combination with a relatively stable allergen. The latter is supported by the positive prick tests with heated grapes as it has been also shown in another patient.3 The negative skin tests to and the clinical tolerance of other grapes suggest a specific allergen in Americana grapes. Aspergillus as a contaminating allergen is unlikely because it was not found on cultured Americana grapes, and skin tests with ethanol-cleaned grapes were also positive. Since the patient has avoided Americana grapes, he has had no further anaphylactic reactions. Some patients with grape allergy have atopic diseases and there appears to be some cross-reactivity to other foods such as cherry,10 plum,3 banana, kiwi, and chestnut7 on the basis of clinical grounds and on RAST inhibition tests. Other patients,8 as our case, have no previous atopic diseases and are monosensitized to grapes. Grapes should be added to the increasing number of fruits that elicit oral allergic symptoms and sometimes more severe reactions such as anaphylaxis. When commercial skin test extracts are negative, fresh grapes should be tested by the prick-to-prick method. REFERENCES 1. Eriksson N. Food sensitivity reported by patients with asthma and hay fever. Allergy 1978;33:189-96. 2. Eriksson N, Formgren H, Svenonius E. Food hypersensitivity in patients with pollen allergy. Allergy 1982;37:437-43. 3. Senff H, Hausen BM, Exner M, Kalveram KJ, Goos M. Pflaumen- und Weintraubenallergie – ein Fallbericht. Pollenassoziierte Obstallergien und ihre Diagnostik. Z Hautkr 1990;66:337-40. 4. Dohi M, Suko M, Sugiyama H, Yamashita N, Tadokoro K, Juji F, et al. Food-dependent, exercise-induced anaphylaxis: a study on 11 Japanese cases. J Allergy Clin Immunol 1991;87:34-40. 5. Guinnepain M-T, Rassemont R, Laurent J. Le raisin est aussi un trophallergène. Rev Fr Allergol 1997;37:400.
J ALLERGY CLIN IMMUNOL VOLUME 104, NUMBER 5
6. Dreborg S, editor. Skin tests used in type I allergy testing [position paper]. Allergy 1989;44(10 Suppl):44-51. 7. Anton E, Jiménez I, Polo F, Picáns I, Sánchez I, Jerez J. Immediate hypersensitivity to grape: study of cross-reactivity with other fruits. Allergy 1997;52(37 Suppl):119. 8. Vaswani SK, Hamilton RG, Carey RN, Chang BW. Anaphylaxis, recur-
1113
rent urticaria and angioedema from grape hypersensitivity [abstract]. J Allergy Clin Immunol 1998;101(Suppl):S31. 9. Romano C, Ferrara A. Food allergy induced by grapes. Allergy 1998;53:93. 10. Giannoccaro F, Munno G, Riva G, Pugliese S, Paradiso M, Ferrannini A. Oral allergy syndrome to grapes. Allergy 1998;53:451-2.